Dynamic Range of Neurofeedback - ULisboa · (Fernado Pessoa) in Livro do Desassossego iii. iv. Abstract Neurofeedback (NF) is an operant conditioning that allows subjects to control

Dynamic Range of Neurofeedback

Cristiana Pires Alves

Dissertation to obtain the Bologna Master of Science Degree in

Biomedical Technologies

Supervisors:

Prof. Dr. Agostinho Cláudio da Rosa

Prof. Dr. Fernando Manuel Fernandes Melício

Examination Committee

Chairperson: Patrícia Margarida Piedade Figueiredo

Supervisor: Agostinho Cláudio Rosa

Member: Benjamin Abraham Ohana

December 2016

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“O oráculo que disse “Conhece-te” propôs uma tarefa maior que

as de Hércules e um enigma mais negro que o da Esfinge.”

Bernardo Soares

(Fernado Pessoa)

in Livro do Desassossego

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iv

Abstract

Neurofeedback (NF) is an operant conditioning that allows subjects to control their brain activity.

Regardless of the abandonment of the first years, recently the scientific community has presented a

renewed interest in NF. One of the technologies most commonly used to perform NF is the

electroencephalogram (EEG), which records electrical fields generated by the synchronous activation

of a neurons population.

NF as been applied as a complementary therapeutic tool in a wide clinical conditions. It has been

also applied in healthy subjects to improve their performances, from sport to music. However,

methodological differences exists between authors.

A better understanding about the working mechanisms of NF is still necessary and this work aims

to explore a new hypothesis through the dynamic range. The dynamic range refers to the variation in

amplitude of brain waves recorded in EEG, i.e., the lowest and highest amplitude possible to achieve.

A complementary goal is the study of the cumulative or cancellation effects of the dynamic range on

behaviour. NF will be used in this work to enhance and to suppress individual alpha band (IAB)

amplitude in the vertex. For that purpose twelve volunteers were randomly divided in two groups. One

group performed a NF protocol to enhance their IAB amplitude followed by a NF protocol to suppress

their IAB amplitude; between each protocol there was a pause of about one month. At the same time,

the other group performed the same protocols but in an inverse order.

The results obtained revealed that both groups were able to perform successfully NF in both

directions. The results of performance tests revealed improvement in mental rotation accuracy in the

first protocol performed by each group. However, only the group that performed first the enhancement

protocol revealed improvement in response time of mental rotation test. After the intervals and after

the opposite protocol, there were no significant changes in tests. This reveals that the improvements

were maintained over time and after the opposite NF training.

In conclusion, the proposed objectives were achieved, nonetheless, further work should be done, in

particular to increase the number of subjects to participate in the experimental study.

Keywords

Neurofeedback, EEG-biofeedback, alpha, individual alpha frequency, dynamic range.

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Resumo

O neurofeedback (NF) é um método de condicionamento operante em que os indivíduos são

treinados para controlar a sua actividade cerebral. Apesar do abandono nos primeiros anos, a

comunidade científica tem demonstrado recentemente um renovado interesse no NF. Uma das

tecnologias mais utilizadas para realizar NF é o electroencefalograma (EEG), que regista os campos

eléctricos gerados pela activação síncrona de uma população de neurónios.

O NF tem sido aplicado como uma ferramenta terapêutica em várias condições clínicas. Tem

também sido aplicada em indivíduos saudáveis para melhoria do seu desempenho, do desporto à

música. Contudo, existem diferenças metodológicas entre autores.

Uma melhor compreensão sobre os mecanismos de funcionamento do NF é ainda necessária e

este trabalho pretende explorar uma nova hipótese através da gama dinâmica. A gama dinâmica

refere-se à variação em amplitude das ondas ondas cerebrais registadas no EEG, ou seja, o maior e

o menor valor de amplitude que são possíveis de alcançar. Um objectivo complementar é o estudo

dos efeitos da gama dinâmica no comportamento.

Este estudo explora a gama dinâmica da banda do alfa individual (IAB) no vértex, através do EEG-

NF. Para esse fim, doze voluntários foram distribuídos aleatoriamente em dois grupos: um grupo

realizou quinze sessões de NF para aumentar a amplitude relativa da IAB, seguidos de uma cerca de

um mês e, para terminar, realizou mais quinze sessões de NF para diminuir a amplitude relativa da

IAB; ao mesmo tempo, o outro grupo executa os mesmos protocolos, mas pela ordem inversa.

Os resultados obtidos revelaram que os dois grupos foram capazes de executar com sucesso os

dois protocolos nas duas direcções. Os resultados obtidos nos testes de performance revelaram que

os dois grupos melhoram a precisão do teste de rotação mental. No entanto, apenas o grupo que

executou o protocolo para aumentar a IAB revelou melhorias nos tempos de resposta do mesmo

teste. Após o intervalo e o protocolo oposto, nenhum teste revelou alterações significativas. Isto revela

que as melhorias obtidas se mantiveram ao longo do tempo e após o treino de NF na direcção

oposta.

De um modo geral, os objectivos propostos foram alcançados, no entanto, será necessário realizar

trabalho futuro, em particular, aumentar o número de indivíduos a participar no estudo.

Palavras-chave

Neurofeedback, EEG-biofeedback, alfa, frequência individual do alfa, gama dinâmica.

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Contents

1.Introduction......................................................................................................................................... 1

1.1.Motivation................................................................................................................................... 1

1.2.Objectives................................................................................................................................... 2

1.3.Dissertation’s Organization.........................................................................................................2

2.Background......................................................................................................................................... 3

2.1.Central nervous system: brain, neurons and fundamental principles..........................................3

2.1.1.Neurons and their proprieties.............................................................................................4

2.1.2.Cortical interaction..............................................................................................................6

2.2.Technologies to access brain functioning...................................................................................6

2.3.Electroencephalogram................................................................................................................8

2.3.1.Frequency components....................................................................................................10

2.4.Neurofeedback.......................................................................................................................... 11

2.4.1.EEG feedback.................................................................................................................. 12

3.State of the art.................................................................................................................................. 14

4.Experimental Study........................................................................................................................... 16

4.1.Participants............................................................................................................................... 16

4.2.The electroencephalogram recording.......................................................................................16

4.3.Experimental design................................................................................................................. 17

4.4.Assessments............................................................................................................................ 20

4.4.1.Digit span.......................................................................................................................... 20

4.4.2.Odd Ball............................................................................................................................ 20

4.4.3.Mental rotation.................................................................................................................. 21

4.4.4.Mental health inventory.....................................................................................................21

4.5.NF training................................................................................................................................ 22

4.6.Statistical analysis.................................................................................................................... 26

5.Results.............................................................................................................................................. 27

5.1.EEG results.............................................................................................................................. 27

5.1.1.IAB in NF training..............................................................................................................30

5.1.2.IAB in resting baselines....................................................................................................32

5.2.Assessment results................................................................................................................... 32

5.2.1.Forward digit span results.................................................................................................33

5.2.2.Backward digit span results..............................................................................................34

5.2.3.Oddball test results...........................................................................................................35

5.2.4.Mental Rotation results.....................................................................................................36

5.2.5.MHI-5 results.................................................................................................................... 38

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6.Discussion........................................................................................................................................ 39

6.1.EEG results.............................................................................................................................. 39

6.2.Assessment tests...................................................................................................................... 39

7.Conclusions and future work.............................................................................................................41

7.1.Conclusions.............................................................................................................................. 41

7.2.Limitations and future work.......................................................................................................41

8.Bibliographic references................................................................................................................... 42

9.Annexes............................................................................................................................................ 45

9.1.Brain regions and associated functions....................................................................................45

9.2.Informed consent...................................................................................................................... 46

9.3.MHI-5........................................................................................................................................ 47

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List of Figures

Figure 1: Cells in the brain..................................................................................................................... 3

Figure 2: Changes of membrane potential during an action potential....................................................5

Figure 3: Changes in membrane potential with increasing strength of depolarization stimulus.............5

Figure 4: Temporal versus spacial resolution of techniques used to assess brain activity.....................7

Figure 5: The first recorded electroencephalogram of a human............................................................8

Figure 6: Schematic drawing of surface and laminar recordings of EEG waves of the cortex...............9

Figure 7: The 10-20 international system of electrode placement.........................................................9

Figure 8: Individual alpha frequency.....................................................................................................11

Figure 9: PubMed search.................................................................................................................... 14

Figure 10: Protocol distribution per groups..........................................................................................17

Figure 11: Protocol scheme of NF protocol...........................................................................................18

Figure 12: EEG signals recorded in a resting baseline with eyes closed selected...............................18

Figure 13: Amplitude map with eyes closed.........................................................................................19

Figure 14: EEG signals recorded in a baseline with open open selected............................................19

Figure 15: Amplitude map with eyes open...........................................................................................19

Figure 16: Digit span test..................................................................................................................... 20

Figure 17: Geometrical figures in odd ball test.....................................................................................21

Figure 18: Mental rotation test.............................................................................................................21

Figure 19: Example of amplitude spectrum used to calculate IAB.......................................................22

Figure 20: Feedback display when NF goal is accomplished more than 2 s.......................................23

Figure 21: EEG signals recorded during a session, with a period of NF goal accomplished selected. 24

Figure 22: Amplitude map while accomplishing NF goal in enhancement protocol..............................24

Figure 23: Feedback display when the goal of NF is not accomplished..............................................25

Figure 24: EEG signals recorded during a session, with a period of NF goal not accomplished

selected................................................................................................................................................ 25

Figure 25: Amplitude map while NF goal in enhancement protocol is not achieved............................25

Figure 26: Amplitude maps during enhancement of IAB in NF.............................................................27

Figure 27: Spectrum of relative amplitude of EEG signal at Cz during NF...........................................28

Figure 28: IAB relative amplitude over sessions in enhancement NF..................................................29

Figure 29: IAB relative amplitude over sessions in suppression NF.....................................................29

Figure 30: Relative IAB amplitude in enhancement NF training over sessions....................................30

Figure 31: Relative IAB amplitude in suppression NF training over sessions.......................................31

Figure 32: Forward digit span results....................................................................................................33

Figure 33: Backward digit span results.................................................................................................34

Figure 34: Oddball results..................................................................................................................... 35

Figure 35: Mental rotation accuracy results..........................................................................................36

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Figure 36: Mental rotation response time results..................................................................................37

Figure 37: MHI-5 response time results................................................................................................38

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List of Tables

Table 1: Training intensity index in groups and protocols......................................................................17

Table 2: Forward digit span results.......................................................................................................33

Table 3: Backward digit span results.....................................................................................................34

Table 4: Oddball accuracy results.........................................................................................................35

Table 5: Mental rotation accuracy results..............................................................................................36

Table 6: Mental rotation response time results......................................................................................37

Table 7: MHI-5 results........................................................................................................................... 38

Table 8: Brain regions, location and associated functions, problems and considerations.....................45

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AcronymsEEG Electroencephalography, Electroencephalogram

EC Eyes closed

EO Eyes open

fMRI Functional Magnetic Resonance Imaging

IAF Individual Alpha Frequency

IAP Individual Alpha Peak

MEG Magnetoencephalogram

MHI-5 Mental Health Inventory – short version with 5 questions

NF Neurofeedback

NIRS Near-Infrared Spectroscopy

PET Positron Emission Tomography

SPECT Single Photon Emission Computer Tomography

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1. Introduction

This chapter has the purpose to present the motivation and the objectives of this work. It is also

explained the organization of this dissertation.

1.1. Motivation

The neurofeedback (NF) training was introduced to the scientific community in the 1960’s by

Joseph Kamiya. (Demos, 2005; J. H. Gruzelier, 2014) NF is the training of brain activity through an

operant conditioning in which some features of neural activity is feed back to the learner (J. H.

Gruzelier, 2014; Marzbani, Marateb, & Mansourian, 2016). Although the first steps in this area were

made about 50 years ago, it was only in the last decade that NF has gained a renovated interest, and

evidence-based applications are growing exponentially (J. H. Gruzelier, 2014).

The electroencephalography (EEG) is the most common technology used to perform NF (Huster,

Mokom, Enriquez-Geppert, & Herrmann, 2014) manly because its advantages: high temporal

resolution, relatively inexpensive, non-invasive, safe, comfortable, and easy to conduct (Gevins, Le,

Brickett, Reutter, & Desmond, 1991; He, Yang, Wilke, & Han Yuan, 2011). The signals recorded with

EEG are the electrical fields produced during the synchronous activation of a population of neurons

(He et al., 2011; Lopes da Silva, 2013), and are traditionally described in terms of frequency (Lopes da

Silva, 2013).

The majority of studies found in the literature with healthy subjects describe NF to increase or to

decrease a brain wave, there are also studies to up-regulate a brain wave while down-regulate

another type of brain wave (Marzbani et al., 2016). However, only a reduced number of studies

performed opposite protocols in the same location but are dated from the 70’s and their

methodological experiment are not clear (Lynch, Paskewitz, & Orne, 1974; Regestein, Pegram, Cook,

& Bradley, 1973).

In order to better understand the working mechanisms of NF, a new hypothesis is put forward

through the dynamic range, i.e., the lowest and highest amplitude possible to be achieved. This work

not only study the bidirectional NF in the same location but also aims to verify the effects of opposite

protocols. In particular, to verify if the effects obtained with one protocol are maintained or cancelled

with the opposite protocol.

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1.2. Objectives

The main objective of this work is to explore the proposed hypothesis, exploring the dynamic range

of NF in healthy volunteers and its effects on performance tests, in order to answer the questions:

1. Can subjects successfully perform NF to increase and decrease NF?

2. The effects obtained through one NF protocol are maintained or cancelled after the opposite

NF protocol?

1.3. Dissertation’s Organization

This dissertation is organized in seven sections to present the work developed in this project.

This first section is used to explain the motivation, expose the problem to be addressed, identify the

objectives of the work, present the project framework and the dissertation organization.

In the second chapter, the basic principles needed to understand the electroencephalogram and

the NF are explained. In the third chapter, a literary review about the state of the art is presented.

In chapter four, it is explained the experimental design used in the project to accomplish the

objectives proposed. And the results are presented in the fifth chapter.

The results are discussed in the following chapter, the chapter number six. In the last chapter,

chapter seven, the conclusions and the project limitations are presents, and also a proposal for future

work.

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2. Background

In this chapter, it will be described the fundamental aspects of brain, its functioning and the

technologies used to access it, where the electroencephalogram is more detailed since it is the

technique used to perform the NF.

2.1. Central nervous system: brain, neurons and

fundamental principles

The human brain is the most complex organ which acts as the centrer of the nervous system (Lu &

Yuan, 2015). In the last years, the knowledge about the brain has evolved significantly – the first

studies started to identify the localization of brain activity and nowadays it is possible to identify and

characterize the brain networks involved in information processing and task performance (He et al.,

2011).

Figure 1: Cells in the brain.

(From (Netter, Craig, & Perkins, 2002).)

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Neurons and glia cells are the main elements of the central nervous system and are organized in a

laminar character (Seeley, Stephens, & Tate, 2005; Speckman, ELger, & Gorji, 2011; Widmaier, Raff, &

Strang, 2004). Figure 1 illustrates the different cells found in the brain.

Neurons, also known as nerve cells, have several processes that emerge from the body, where the

nucleus is contained. Most of these processes are dendrites, which are branched into small

ramifications, and one of the processes is the axon, which may split into multiple collaterals to contact

with another neuron or a target organ. Each neuron is also covered with several thousands of

synapses, which are an anatomically specialized junction where a neuron releases neurotransmitters

to communicate to another one (Seeley et al., 2005; Speckman et al., 2011; Widmaier et al., 2004).

Glia cells, such as astrocytes and oligodendrocytes, are embedded between the neurons. The glia

cells have several processes that make contact with neurons and vessels. The cerebral extracellular

space have a very narrow intercellular space (Seeley et al., 2005; Siegel & Sapru, 2006; Speckman et

al., 2011; Widmaier et al., 2004).

2.1.1. Neurons and their proprieties

Neurons are the basic unit of the nervous system and operate through the generation of electrical

signals that pass from one part of the cell to another part of the same cell releasing chemical

messengers, called neurotransmitters, to communicate with other cells. The output of the neuron is the

result of thousands or even hundred of thousands of inputs received from other neurons (Seeley et al.,

2005; Widmaier et al., 2004).

The membrane potential, which can be recorded with a microelectrode placed in the intracellular

space, has a potential about 60-70 mV, with a negative polarity, which is the result of concentration

gradients of different ions, particularly sodium and potassium. The potential of the membrane is

subject to various fluctuations mainly elicited by the synaptic activities (Seeley et al., 2005; Widmaier

et al., 2004).

When a neuron is excited it can initialize a depolarization of the membrane, also known as the

action potential. During the action potential the membrane potential may change 100 mV, from -70 mV

to +30 mV (figure 2) (Seeley et al., 2005; Speckman et al., 2011; Widmaier et al., 2004).

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Figure 2: Changes of membrane potentialduring an action potential.

(From (Vander et al., 2001).)

Action potentials are all-or-none responses (figure 3), which means that, regardless of the size of

the stimulus, if the membrane potential reaches the threshold it initializes an action potential which has

always the same size. The threshold is usually 15 mV less negative than the resting membrane

potential. In other words, the action potentials either occur maximally or do not occur at all (Seeley et

al., 2005; Widmaier et al., 2004).

Figure 3: Changes in membrane potential with increasingstrength of depolarization stimulus.

(From (Vander, Sherman, & Luciano, 2001).)

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Once the action potential is initialized it is propagated along the membrane until it reaches the

other end of the nerve cell (Seeley et al., 2005; Widmaier et al., 2004).

2.1.2. Cortical interaction

The neurons interact with each other and their connectivity can be described as anatomic,

functional and effective connectivity. The anatomic connectivity refers to physical neural connections

between regions of interest at micro- or macroscopic level. The microscopic level include dendritic

sprouting and the synaptic connections while the macroscopic level embrace the tracts that connect

spatially different brain regions. The functional and effective connectivity are based in the functional

proprieties of various cortical regions instead of the physical connection between them. The functional

connectivity is defined as the temporal correlations between spatially remote neurophysiological

events whereas the effective connectivity is defined as the influence that one neural system exerts

over another either directly or indirectly. In other words, the functional connectivity accounts for the

statistical association between two neuronal activities while the effective connectivity accounts for the

causal influence of one system on another (He et al., 2011; Lopes da Silva, 2013).

2.2. Technologies to access brain functioning

Nowadays it is possible to gain insight of the brain’s activity through several methods: functional

magnetic resonance (fMRI) (He et al., 2011), near infrared spectroscopy (NIRS) (Naseer & Hong,

2015), positron emission tomography (PET) (Gevins et al., 1991), single photon emission computed

tomography (SPECT) (Lu & Yuan, 2015), magnetoencephalography (MEG), and

electroencephalography (EEG) (Gevins et al., 1991; He et al., 2011). Each of these methods vary in

terms of temporal and spacial characteristics (Gevins et al., 1991; He et al., 2011; Naseer & Hong,

2015). There are also some studies that use multimodal neuroimaging integrating two techniques in

order to avail the best characteristics of each, as combining fMRI and EEG, or fMRI and MEG (He et

al., 2011), or NIRS and EEG (Naseer & Hong, 2015). The figure 4 illustrates the differences between

these methods according to spatial and temporal resolution (He et al., 2011).

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Figure 4: Temporal versus spacial resolution oftechniques used to assess brain activity.

(Adapted from (He et al., 2011).)

The fMRI measures the cerebral haemodynamic changes which arise from the neuronal activity.

One of the major advantages of this technique is the ability of acquire images of the entire cerebral

volume. It also has the advantage of having a non-invasive basis. Although the data recorded does not

arises from the neuronal activity, it is possible to indirectly measure it. In contrast to its high spatial

resolution, it has a low temporal resolution (He et al., 2011).

NIRS is an optical spectroscopy method that makes use of the optimal light absorption proprieties

of haemoglobin in order to measure changes in cerebral haemodynamic and infer about neural

activity. Similar to fMRI but with lower spatial resolution, NIRS infers indirectly about neuronal activity

(Naseer & Hong, 2015). This technique is called by some authors as hemoencephalography

(Budzynski, Budzynski, Evans, & Abarbanel, 2009).

The PET and SPECT evaluate the physiological function and biochemical changes of molecular

targets through the measurement of radionuclide decay. Both methods have a high sensitivity, good

spacial resolution and limitless penetration depth (He et al., 2011).

In PET a pair of high energy γ-rays emitted indirectly from a radioisotope are recorded. The

radioisotopes are produced in a huge and high-cost cyclotron and introduced quickly into the subject

due to its short half-life. Through the computer analysis it is possible to obtain three-dimensional

images of functional processes (He et al., 2011).

Similar to PET, SPECT also uses a radioactive tracer and detection of γ-rays. However, the

radioisotopes used for SPECT emit only a single γ-rays during decay. The nuclides used have longer

half-life and it is less expensive than PET but the spatial resolution of SPECT is lower compared to

PET (He et al., 2011).

Finally, MEG and EEG record magnetic and electrical fields, respectively, that are generated by the

ionic currents generated by biochemical processes at cellular level when a population of neurons are

activated synchronously. Both methods are non-invasive and have a high temporal resolution (Lopes

da Silva, 2013; Schomer & Lopes da Silva, 2011).

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2.3. Electroencephalogram

The EEG was described for the first time by Hans Berger in 1929 as the record of brain electrical

fields (Hans, 1929; Lopes da Silva, 2013; Niedermeyer & Schomer, 2011). The main sources of the

referred electrical fields are the ionic currents generated by biochemical processes at the cellular level

(Lopes da Silva, 2013). The electroencephalogram reflects the electrical activity underneath the parts

where the electrodes are placed, specifically the synchronous activity of a specific type of neurons, the

pyramidal neurons of the cortex (Lopes da Silva, 2013; Speckman et al., 2011).

Figure 5: The first recorded electroencephalogram of a human.

(From (Hans, 1929).)

The pyramidal neurons of the cortex are arranged in the form of palisade, with the main axes of

their dendritic trees parallel to each other and perpendicular to the cortical surface. When these

neurons are activated, intra- and extracellular currents flow; the longitudinal components of these

currents add, whereas their transverse components cancel. The result is a laminar current log along

the main axes of the neurons. This laminar current generates simultaneously electrical and magnetic

fields. When the neurons are in synchronized activation, forming dynamic assemblies, the electro-

magnetic fields created can be recorded at a distance (He et al., 2011; Lopes da Silva, 2013;

Speckman et al., 2011).

The EEG records the local field potentials from the electrical field potentials which represents the

mainly the extracellular currents, and the magnetoencephalogram records the local magnetic fields

which represents mainly the primary intracellular currents. The main sources of the signals recorded

by these technologies are essentially the same – the ionic currents generated by biochemical

processes at the cellular level (Lopes da Silva, 2013). Although the EEG and the MEG are very closed

methodologies, the first is the one that has been used in this work and will be the focus of this section.

The neuronal signals reach the scalp passing through several layers of tissues with different

proprieties – cerebrospinal fluid, skull, and skin – implying a distortion in the signals recorded from the

scalp (Lopes da Silva, 2013), as shown in figure 6.

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Figure 6: Schematic drawing of surface and laminar recordings ofEEG waves of the cortex.

In 1 is a recorded signal from the surface, and in 1, 2, 3, 4, 5 and6 are recordings from deeper layers – from a rat’s motor cortex.

(From (Speckman et al., 2011).)

In order to record the EEG signal, several electrodes are placed in the scalp following the rules

from the 10-20 international electrode placement system, proposed by Jasper in 1958. In this system,

the electrodes are placed at relative distances of 10 and 20%, and their locations are named using a

letter and a number (Budzynski et al., 2009; Schomer & Lopes da Silva, 2011). In figure 7 is

represented the rules for placing the electrodes.

Figure 7: The 10-20 international system ofelectrode placement.

(From (Ebersole et al., 2014)).

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The letters refer to the region of the brain underneath the electrode: F (frontal), P (parietal), T

(temporal), O (occipital), C (central). The numbers identify the hemisphere: the odd numbers refers to

electrodes placed in the left side of the head, and the even number refers to electrodes placed in the

right side of the head. If the number is replaced by the letter z, it indicates that the electrode is placed

in central line between nasion and inion. Some additional electrodes are placed sometimes, e.g., A1

and A2 (left and right auricular, respectively), or M1 and M2 (left and right mastoid process,

respectively) (Budzynski et al., 2009; Marzbani et al., 2016; Speckman et al., 2011).

The number of electrodes used at one time depend on the type of research being done, even more

electrodes can be placed, using the 10-10 system, for example (Ebersole, Nordli Jr., & Husain, 2014).

2.3.1. Frequency components

The EEG signal contains superimposed oscillations in a wide range of frequencies. In humans,

those oscillations range between 0,05 to 600 Hz. However, when the EEG is recorded from the scalp,

the frequencies are typically limited under 30 Hz (Ebersole et al., 2014).

Traditionally, the EEG is described in terms of frequency, classically defined as: infraslow (inferior

to 0.2 Hz), delta (from 0.2 to 4 Hz), theta (from 4 to 8 Hz), alpha and mu (from 8 to 13 HZ), beta (from

14 to 30 Hz), gamma (from 30 to 90 Hz), and high-frequency oscillations (superior to 90 Hz) (Lopes da

Silva, 2013). These different patterns are known as known as brain waves (Marzbani et al., 2016).

However, different authors define brain waves bands slightly different.

In a general overview, delta waves dominates the EEG in deep sleep, theta in drowsiness, alpha in

wakefulness relaxation, beta in concentration and alertness, gamma in problem resolution. This may

indicate that higher frequencies are related with higher alertness from individuals, nevertheless it is

inappropriate to associate the frequency bands with a single function – it may reflect different states

and types of communication resulting from different sources during different tasks (Budzynski et al.,

2009; J. Gruzelier & Egner, 2005; Marzbani et al., 2016).

Concerning the alpha frequency, different authors define different limits. Some authors define alpha

waves in a range between 8 and 13 Hz, while others define it between 8 and 12 Hz, or other slightly

differences. A simple solution to the definition of alpha is to use the individual alpha for each

participant (Klimesch, 1999).

Recently, a growing number of studies started to use individual alpha frequency band (IAB),

adjusting individually the training. In this way, it is possible to increase the effectiveness of NF

(Bazanova & Mernaya, 2008). IAB can be determined by plotting the EEG spectrum from a record with

eyes opens and a record with eyes closed. This plot allows to identify the peak of alpha frequency and

the boundaries, as well to determine the other frequency bands, as possible to observe in figure 8.

The limits of alpha frequency are defined according to the peak alpha frequency: the upper limit is the

peak alpha frequency adding 2 Hz, and the lower limit is the peak alpha frequency subtracting 4 Hz

(Klimesch, 1999).

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Figure 8: Individual alpha frequency.

(Image adapted from (Klimesch, 1999).)

The frequency bands can also be divided in sub-bands, usually defined as high or low, according to

their frequencies. These sub-bands are reported both in classical definition of alpha (Cremades &

Pease, 2007) and individual alpha definition (Klimesch, 1999). Regarding the IAB and its sub-bands:

the high alpha is defined between the peak alpha frequency and the upper limit, and low alpha is

defined between the peak alpha frequency and the lower limit. The lower alpha integrates two further

bands: lower alpha 1 and lower alpha 2 (figure 8) (Klimesch, 1999).

2.4. Neurofeedback

Neurofeedback (NF) is a form of biofeedback, an operant conditioning that assists the subject to

control their brain waves (Demos, 2005; Marzbani et al., 2016). The first works in NF were developed

in 1963 by Joseph Kamiya: he trained a volunteer to recognize bursts of alpha waves and gave verbal

reinforcement each time he achieved to produce those waves (Demos, 2005).

The work of Kamiya demonstrated the typical biofeedback loop – an instrument records a specific

activity of interest, a trainee is reinforced (fed back) each time the desired activity occurs, and then it is

possible to voluntarily control the biological activity (Demos, 2005; Marzbani et al., 2016). It is possible

to identify five elements in a NF system: 1) brain signal acquisition, 2) signal processing, 3) feature

extraction, 4) generation of the feedback signal, and 5) an adaptive learner (Huster et al., 2014). The

feedback signal can be in form of audio, visual, or a combination of both (Marzbani et al., 2016).

The foundations of NF rely in two facts: the brain state can be objectively reflected in parameters

recorded from the scalp, and the brain has plasticity to memorize the desired (and thereby, rewarded)

state of the brain. Based in these facts, NF trains individuals to regulate their brain activity in response

to real-time feedback (Kropotov, 2009).

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NF has been applied not only in several disorders but also in healthy subjects. There are

successful reports in attention deficit hyperactivity disorder, epilepsy, autistic spectrum, anxiety,

depression, amongst others. Taking in consideration the fact that there is no side effects registered to

date, NF has been an interesting complement to the treatment of the clinical conditions mentioned

(Budzynski et al., 2009; Demos, 2005; Marzbani et al., 2016).

In healthy populations, the objective of NF is to optimise the performance in different areas. The

main areas where NF is used to optimise the performance are for sport, musical and artistic

performance, and cognitive performance (Budzynski et al., 2009; Demos, 2005; Marzbani et al., 2016).

Between the technologies mentioned to assess brain functioning, only EEG, MEG, fMRI, and NIRS

have been used in NF training until now (Gevins et al., 1991; Okazaki et al., 2015). The EEG has

higher temporal resolution, is relatively inexpensive, and is more comfortable for the patients. These

advantages makes the EEG-biofeedback, i.e., NF with EEG, the modality more used in this field

(Gevins et al., 1991). Since the EEG is the technique used in this project, from this part of the

dissertation whenever the term neurofeedback is used it refers to EEG-biofeedback.

2.4.1. EEG feedback

In the literature it is possible to find different electrode placements and different wave bands to be

trained with EEG signals. The NF training consists in increase and/or decrease a specific frequency

band at a previously defined location (Budzynski et al., 2009).

Although it is possible to record a full EEG (with all 10-20 electrodes), it is commonly used only one

single active electrode to perform the NF training. The montages traditionally applied can be unipolar

or bipolar (Demos, 2005; Evans & Abarbanel, 1999; Marzbani et al., 2016).

In a unipolar montage, the active electrode is placed in the scalp and the reference electrode is

placed outside the scalp. The signal to be used in NF is obtained by subtracting the activity of the

reference electrode from the brain activity of the active electrode (Demos, 2005; Evans & Abarbanel,

1999; Marzbani et al., 2016).

On the other hand, in the bipolar montage, two electrodes are placed on the scalp. The difference

between the brain signals of those electrodes is the signal to be used in NF (Demos, 2005; Evans &

Abarbanel, 1999; Marzbani et al., 2016). This montage has the advantage is the common mode

rejection, which means that any external artifact occurring in both channels at the same time is

subtracted in amplitude and phase, improving spatial selectivity (Evans & Abarbanel, 1999; Marzbani

et al., 2016).

The selection of active electrode placement to perform NF depends on the objective of the training.

Over the years, neuroscientists have associated brain areas with certain cognitive functions (see a

detailed description of in annex 9.1). When a NF training is designed It is necessary to take in

consideration the sites and the cognitive functions under them (Demos, 2005; Marzbani et al., 2016).

12

Besides the localization of the active electrode, it is also necessary to choose the frequencies to be

modulated. It could be trained the full range of a defined brain wave, or a sub-band. It can also be

trained two brain waves in opposite directions; the alpha/theta NF is a common used protocol. Again,

the choose of the frequencies to be modulated depend on the objective of the study, taking in

consideration the states or functions that each one is associated (Marzbani et al., 2016; Rogala et al.,

2016).

The threshold criteria is also important, since the feedback information to the subject depends on it.

The threshold comprises the characteristics of the brain waves training to be accomplish, usually it is

defined in amplitude and/or percent of time spent above or under that amplitude (Demos, 2005). In the

studies explored, the threshold varies with among the different authors. And some authors do not

define the threshold, or it is unclear.

Other issues should be considering in the design of the protocols: if it will be realized with eyes

closed or eyes open; if the feedback will be visual, audio, or audio-visual. And also, the training regime

is also important, and comprises the trial length, the session length, the number of training sessions

needed, the training schedule. NF is usually administered twice per week, and each session last one

hour including the preparation time. Typically, each session has twenty to forty minutes of NF. The

number of sessions varies accordingly to each participant learning success, condition to be treated,

and severity of that conditions, among other factors (Angelakis et al., 2007).

Although the divergences between authors in methodological aspects, NF has been reported as

useful tool in clinical and non-clinical fields (Budzynski et al., 2009; J. H. Gruzelier, 2014; Marzbani et

al., 2016). In the clinical application of NF, there are successful results in conditions such as attention

deficit hyperactivity, autism spectrum disorder, depression, epilepsy, schizophrenia, insomnia, drug

addition, anxiety, stroke, eating disorders (J. H. Gruzelier, 2014; Marzbani et al., 2016). The interest in

non-clinical fields had increased in the last years and it is possible to find successful reports in the

literature, such as: memory (J. H. Gruzelier, 2014; Klimesch, 1999; Nan et al., 2012); musical

performance (Bazanova & Mernaya, 2008; Markovska-Simoska, Pop-Jordanova, & Georgiev, 2008);

surgical performance (Ros et al., 2009); sport performance (J. H. Gruzelier, 2014; Thompson, Steffert,

Ros, Leach, & Gruzelier, 2008).

13

3. State of the art

NF has been utilized since the 1960’s (Demos, 2005), although its interest has decreased during

the 1980’s and 1990’s. Recently, the interest in NF has increased. The latest search in PubMed

(https://www.ncbi.nlm.nih.gov/pubmed – a free resource that is developed and maintained by the

National Center for Biotechnology Information, NCBI, at the United States National Library of

Medicine, NLM, located at the National Institutes of Health, NIH) for this project was made on

November 17, 2016, using the terms “neurofeedback” and “EEG biofeedback” revealed a growth in the

number of papers published in this field, as can be observed in figure 9.

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Figure 9: PubMed search.

PubMed search with the terms "neurofeedback" and "EEG biofeedback" on November 17, 2016.

When the same terms were searched in Google Scholar (https://scholar.google.pt/), the number of

results were superior. The search with the term “neurofeedback” obtained about 23000 results from

any time and about 2130 results from 2016. Whilst the search with the term “EEG feedback” presented

about 522000 results from any time and about 15400 results from 2016.

The studies founded in the research of the state of the art in healthy subjects identify a whole range

of cognitive abilities linked to the alpha waves: musical performance (Bazanova & Mernaya, 2008;

Markovska-Simoska et al., 2008), mental rotation (Hanslmayr, Sauseng, Doppelmayr, Schabus, &

Klimesch, 2005; Zoefel, Huster, & Herrmann, 2011), speed of processing (Angelakis et al., 2007),

14

https://scholar.google.pt/

https://www.ncbi.nlm.nih.gov/pubmed

memory performance (Angelakis et al., 2007; Escolano, Aguilar, & Minguez, 2011; Nan et al., 2012),

mood (Schmeidler & Lewis, 1971), perception of time (Wacker, 1996).

Using NF to only decrease alpha is only reported in a few studies. One study with healthy subjects

reported high creative outcome associated to the suppression of alpha (Martindale & Armstrong,

1974).

Relatively to studies in which the same subject performs both protocols at the same location, the

few works founded are dated from the 1970’s. One study (Regestein et al., 1973) reported 12

continuously hours of NF to enhance alpha and one week later another 12 hours of NF to suppress

alpha. Although it was not clear the methodological design, like the threshold or the definition of alpha,

the authors of that study reported that it was not possible to predict the success of the second protocol

based in the information collected in the first one. In the next year, (Lynch et al., 1974) indicated that

there was a negative correlation between the two protocols, i.e., the participants that reported the

enhancement NF easier founded suppression NF harder, and vice versa. Once again the

methodological experiment was not clear.

No other studies where found describing NF training in different directions, in the same location,

and in the same subjects. The work developed and presented in this thesis could fill the gap in the

literature.

15

4. Experimental Study

In order to explore the hypothesis proposed, it was designed a study with healthy participants that

performed NF to enhance and to suppress their IAB. The study will be described in detail in this

chapter.

4.1. Participants

For this study, twelve healthy adult subjects volunteered, and gave their written consent. The

exclusion criteria included:

• Age under 18;

• Neurological, Psychiatric or Psychological disorders;

• Use of chronic medication or addictive drugs;

• No previous NF training.

The subjects, 5 males and 7 females, had between 23 and 44 years old (mean of 29,83 and

standard deviation of 6,29). They were randomly distributed in two groups – each group performed a

different NF protocol, which are described later in this chapter.

4.2. The electroencephalogram recording

The electroencephalographic signals were acquired through electrodes placed in the head

accordingly to the 10-20 system. A cap with 20 electrodes was used to place the majority of the

electrodes, and three additional electrodes were also placed: two reference electrodes were placed in

M1 and M2 (above the left and right mastoid process, respectively), and a ground electrode in the

forehead. It was necessary to place a conductive gel between the skin and the electrodes.

In order to amplify the signals, it was used the amplifier Vertex 823 (from Meditron Electromedicina

Ltda, SP, Brazil) composed by the hardware EEG Compact 723, with the an analogical band-pass filter

between 0,1 and 70 Hz.

The signals were recorded by Somnium software platform (Cognitron, SP, Brazil), with a sampling

rate of 256 Hz. The electrodes were kept with a circuit impedance below 10 kΩ.

16

4.3. Experimental design

The participants were randomly distributed in two groups. Each group consisted of 6 subjects, with

no significant difference in age or gender. Group 1 had 3 males and 3 females (age mean of 29,67

years old and standard deviation of 7,840), and group 2 had 2 males and 4 females (age mean of

30,00 years old and standard deviation of 5,060).

Group 1 started with a NF protocol to enhance the IAB in the vertex (Cz). After this protocol the

subjects performed a new NF protocol to suppress the IAB in the same region. Between each protocol

there was an interval (four to five weeks), during this period there was no NF training nor

assessments. At the same time group 2 performed the same protocols but in the inverse order – the

first protocol that this group performed was to suppress IAB at Cz, and their second protocol was to

enhance this band in the same location. The figure 10, illustrates the distribution of the protocols in the

groups.

During the experimental study some subjects did not completed the two protocols: in group 1, two

subjects did not started the second protocol; in group 2, one subject did not started the second

protocol and another subject only performed 7 sessions in the second protocol.

Both protocols were organized equally – they only differ in the direction of NF (enhancing or

suppressing IAB). Each protocol was composed with fifteen sessions and the subjects were asked to

perform two sessions per week.

Although each subject was asked to perform two sessions per week, due to personal schedules,

the intensity of training (i.e., the total number of training days divided by the average interval, in days,

between them) was slightly different between each subject. The table 1 present the intensity mean

values in each group and protocol.

Table 1: Training intensity index in groups and protocols.

Group 1 Group 2 Both

Protocol to enhance IAB 3,5 3,33 3,45

Protocol do suppress IAB 3,42 4,12 3,80

Both 3,47 3,84

17

Figure 10: Protocol distribution per groups.

In the first session, the volunteers were instructed to perform a resting baseline, followed by

performance tests, NF training, and finally another resting baseline. From the second to the fifteenth

sessions, the sessions were composed with a resting baseline, followed by the NF training, and

another resting baseline. In fifth, tenth, and fifteenth sessions after the post-NF baseline it was applied

the same performance tests of the first session, in order to evaluate the effects of NF over sessions.

The protocol organization can be visualized in the figure 11.

Figure 11: Protocol scheme of NF protocol.

In the resting baseline, the subjects were asked to keep their eyes open (EO) for one minute, then

one minute with eyes closed (EC), and this sequence was repeated one more time. The first resting

baseline was used to determine IAB. The figure 12 shows the signals recorded in a subject during a

baseline in a 15 s window. In this window it is also selected a period of 1 s during EC baseline, that it

is used extract the amplitude maps presented in figure 13. The figure 14 shows the same temporal

window from figure 12, but the selected period is in EO baseline, and its amplitude maps are

presented in figure 15.

Figure 12: EEG signals recorded in a resting baseline with eyes closed selected.

Window with 15 s.

18

Figure 13: Amplitude map with eyes closed.

From the area selected in figure 12.

Figure 14: EEG signals recorded in a baseline with open open selected.

Window with 15 s.

Figure 15: Amplitude map with eyes open.


19

The assessment tests realized to evaluate the effects of NF in the subjects included: normal digit

span, reverse digit span, oddball, mental rotation. It was also applied a mental health questionnaire.

The NF training involves five blocks of trials. Each block was constituted by five trials – each trial

lasts one minute – with five seconds between trials. In this way each session has 25 minutes of

effective NF training, and each protocol 375 minutes (6,25 hours).

4.4. Assessments

On first, fifth, tenth, and fifteenth sessions, subjects were asked to perform assessment tests in

order to evaluate the effects of NF training. Each of those tests will be explained in the following

subsections.

4.4.1. Digit span

The digit span, which is the maximum number of digits a person can recall in the correct order, and

it is widely used to assess memory (Nan et al., 2012). The test (figure 16) consisted in a series of trials

showing digits randomly, and the subjects were asked to repeat them in the same or reverse order,

performing forward or backward digit span, respectively. The amount of digits displayed started with

two and finished with ten in the first assessment of each protocol; in the following assessments, it

started with five and finished with fifteenth.

Figure 16: Digit span test.

4.4.2. Odd Ball

The odd ball test is used to evaluate the attention of the subjects. In this test, different geometrical

forms appear – those forms consist in a circle, an octagon and a square (figure 17) – and the

volunteers where instructed to click only if the circle appear. The test consisted in 50 trials, where the

images appeared during 0,5 s with an interval of 0,5 s. It was defined a decoy rate of 40 %.

20

Figure 17: Geometrical figures in odd ball test.

4.4.3. Mental rotation

The mental rotation test is another test commonly used to measure the cognitive performance in

subjects, (Hanslmayr et al., 2005; Zoefel et al., 2011). In this test, two dimensional objects are

displayed side by side (figure 18) and the subject is instructed to answer if the two objects are the

same but rotated in a certain axis, or if the objects are mirrored but also rotated. The test consisted in

20 trials, where the images are shown during 7 s with an interval of 3 s. The answer should be given

during those 7 s when the images appear.

Figure 18: Mental rotation test.

4.4.4. Mental health inventory

The mental health inventory (MHI) is a self-report developed as a tool to evaluate psychological

distress and well-being in the population. This test includes thirty-eight questions and was validated to

the Portuguese population. Each question has five of six items that have a value in an ordinal scale –

a higher in the result of the questionnaire corresponds to a higher mental health (Ribeiro, 2001). Since

the extended version could be a discouraging factor, in this study it was used the short version, with

five questions (MHI-5). Although the reduced number of questions, it has a high correlation with the full

version. The MHI-5 can be consulted in the annex 9.3.

21

4.5. NF training

Independently of the protocol applied, the NF training was performed at the vertex, which

corresponds to the electrode Cz. It was also used the same EEG frequency band in both protocols:

IAB.

The IAB band was calculated with the data from EEG signal at Cz collected in the first baseline.

Using the spectrum of the signal with the eyes open and with the eyes closed, it was possible to

determine the limits of IAB band, which correspond to the crossing of the spectrum with the eyes open

and with the eyes closed. The lower limit corresponds to the lower transition frequency (LTF) and the

higher value corresponds to the higher transition frequency (HTF). The highest value of amplitude

within those limits corresponds to the individual alpha peak (IAP) (Klimesch, 1999). The figure 19

demonstrates the boundaries of IAB and the IAP.

Figure 19: Example of amplitude spectrum used to calculate IAB.

The green line corresponds to the spectrum of the signal with eyes closed, and the grey linecorresponds to the spectrum of the signal with eyes open. The IAB ranges between LTF and

HTF, and its higher amplitude corresponds to IAP in IAB.

The relative amplitude of IAB was the parameter defined for the training, and was calculated using

the equation 1. In this equation, f Initial and f Final are the boundaries of IAB, X (k) is the

frequency amplitude spectrum where k is a frequency bin and delta is the relation between

frequency bin and frequency measured in Hz.

22

Equation 1: Equation to calculate relative IAB amplitude.

From (Rodrigues, 2009).

During NF, the amplitudes were obtained by the Fast Fourier Transformation (FFT) in a sliding

window of 2 s that changes every 0,125 s using the last 512 samples. Since the EEG sampling rate

was of 256 Hz, the frequency resolution was 256/512=0,5 Hz.

The feedback information that the subjects received consisted in two objects: a sphere and a cube

(figure 20). Both objects reflected the feedback parameter in real time accordingly to the threshold and

direction defined. In the case of the protocol to increase IAB, the goal is to maintain the relative IAB

above the threshold defined; while in the protocol to decrease IAB, the goal is to keep it below the

threshold. Independently of the protocol, the sphere is rose and bigger if the goal defined is

accomplished, and if it is continuously achieved for more than 2 s, the cube ascends, like it is shown in

figure 20. The figure 21 shows the EEG signals from a session in the protocol to enhance IAB; it is

selected a period while the goal is being achieved to present the amplitude maps (figure 22).

Figure 20: Feedback display when NF goal is accomplished morethan 2 s.

23

Figure 21: EEG signals recorded during a session, with a period of NF goal accomplished selected.

Window with 15 s.

Figure 22: Amplitude map while accomplishing NF goal in enhancement protocol.


Window with 15 s.

When the goal stops being achieving, the sphere becomes white and smaller, reducing the number

of slices – it can even resemble a cube instead. At the same time, if the cube is in an elevated

position, it starts to fall. The figure 23, represents a feedback in which the subject does not

accomplished the goal of NF. The figure 24 shows the EEG signals from a session in the protocol to

enhance IAB; it is selected a period while the goal is being achieved to present the amplitude maps

(figure 25).

24

Figure 23: Feedback display when the goal of NF is notaccomplished.

Figure 24: EEG signals recorded during a session, with a period of NF goal not accomplished selected.

Window with 15 s.

Figure 25: Amplitude map while NF goal in enhancement protocol is not achieved.


25

The participants were informed of the objective of the protocol realized in each session and were

instructed to apply mental strategies in order to increase the sphere size and keep the cube high if

possible. In the first session of each protocol, the threshold was defined as 1, increasing or decreasing

0,1 accordingly to the protocol and success of the previous session.

4.6. Statistical analysis

In first instance, it was calculated the IAB relative amplitude in NF training and in resting baselines

over sessions for all subjects and for each group. In resting baselines it was calculated the IAB relative

amplitude in EO and EC before and after NF. The association between the relative amplitude of IAB in

each period over session was investigated with the Pearson product-moment correlation coefficient

(Pearson correlation, for short).

After the analysis to EEG signals, it was examined the results of the tests in order to verify if there

was any change in each group and protocol. For each test it was conducted a repeated measures

analysis of variance (ANOVA) with time (test 1, 2, 3, and 4) as within-subjects factor and group (group

1 and 2) as between-subjects factor. Then, it was verified if the variables presented a normal

distribution with Shapiro-Wilk test. With normal distribution variables it was used parametric tests,

specifically 1-tailed paired t-test. When normal distribution of data was not found, it was applied non-

parametric test was, namely the Wilcoxon signed-rank test.

All statistic tests applied used a confidence interval percentage of 95%.

26

5. Results

In this chapter, the results obtained will be presented in two subchapters. In the first subchapter it

will be presented the analysis to EEG signals during each NF training and in resting baselines. The

second subchapter present the results of the repeated measures performed in each assessment.

5.1. EEG results

The main focus of this analysis is the relative amplitude of IAB at Cz, although other bands and

regions present variations during NF, as can be observed in the amplitude maps (figure 26) and in the

spectrum of frequencies at Cz (figure 27).

Figure 26: Amplitude maps during enhancement of IAB in NF.

The images A and B represent the amplitude maps during an enhancement NF training of IAB when the goalis not accomplished in two different perspectives but at the same time. While images C and D represent the

amplitude maps during the same protocol when the goal is being achieved. Both maps represent signalsfrom the same subject and in the same session.

27

A B

DC

Figure 27: Spectrum of relative amplitude of EEG signal at Cz during NF.

The spectrum presented in A represents the signals in enhancement NF protocol when the goalis not being achieved. While the spectrum presented in B represents the signals duringaccomplishement of NF goal in the same protocol. EEG signals selected to obtain these

spectrum's can be observed in figures 24 and 21, respectively. The spectrum represented in thisimage correspond to the same period of failure and success represented in the figure 26.

Focusing now in IAB relative amplitude, it will be analysed in two main periods. The first period is

during NF training, in order to verify if the subjects can learn how to successfully change their IAB in

the direction defined in each protocol. The second period refers to baselines recorded before and after

each NF session. Each baseline also has two periods to be analysed, during EO and EC. The period

of EO baseline before and after NF will be named EO pre-NF and EO post-NF. The same will be

applied in EC baselines, EC pre-NF and EC post-NF. Figures 28 and 29 presents IAB relative

amplitude variations in each period for enhancement and suppression NF protocols, respectively, not

considering the groups.

To better understand those variations and the differences in each group, a detailed statistical

analysis was executed and presented in the following subchapters.

28

A

B

Figure 28: IAB relative amplitude over sessions in enhancement NF.

Figure 29: IAB relative amplitude over sessions in suppression NF.

29

5.1.1. IAB in NF training

The average relative amplitude of IAB in each group showed variations over sessions according to

the protocol performed. Figures 30 and 31 present the relative IAB amplitude variation in each NF

protocol for all subjects and in each group and the correspondent linear regression. It is also

presented the linear regression that shows a positive relation between IAB relative amplitude over

session for enhancement NF and a negative relation in suppression NF. The Pearson correlation was

calculated to better understand these results.

Figure 30: Relative IAB amplitude in enhancement NF trainingover sessions.

30

Figure 31: Relative IAB amplitude in suppression NF training oversessions.

Both protocols had high correlation in the direction of the NF training, which were statistically

significant – r = 0,928 and p < 0,001 in enhancement protocol, and r = -0,760 and p = 0,001 in

suppression protocol. However, the correlation is not statistically significant in both groups.

Group 1 had a strong and statistically significant positive correlation (r = 0,614, p = 0,015) in

enhancement NF but in suppression protocol although the correlation was moderate and negative, it

was not statistically significant (r = -0,393, p = 0,148). Whilst group 2 had statistically significant

correlation in both NF protocols – positive correlation for enhancement training (r = 0,922, p < 0,001)

and negative correlation for suppression training (r = -0,639, p < 0,010).

31

5.1.2. IAB in resting baselines

The average IAB amplitude in resting baselines was calculated in baselines with EO and EC.

Pearson correlation was calculated to determine the association between the IAB amplitude in those

periods over sessions. In EC, the correlation calculated was low or moderated and not statistically

significant. Nonetheless, it was found a strong and positive correlation between EO and number of

session in both protocols, not considering the groups.

In enhancement protocol, EO presented r = 0,861 (p < 0,001) in pre-NF and EO presented

r = 0,674 (p = 0,006) in post-NF. Whilst suppression protocol, EO presented r = 0,552 (p = 0,033) in

pre-NF and EO presented r = 0,521 (p = 0,046) in post-NF.

However, the changes in EO baselines differs in each group. In group 1, the high and strong

correlation is observed in enhancement protocol (r = 0,856, p < 0,001 in EO pre-NF and r = 0,773,

p = 0,001 in EO post-NF); whereas in group 2, it is observed in suppression protocol (r = 0,552,

p < 0,033 in EO pre-NF and r = 0,589, p = 0,046 in EO post-NF). Although the NF are not the same, it

should be stressed that it was the first protocol performed by each group.

5.2. Assessment results

The tests performed in each assessment included forward and backward digit spas, oddball and

mental rotation. It was also included the MHI-5. In this subsection, each assessment will be presented.

Each assessment was performed four time in each protocol: in the first session, before NF; and in the

end of the fifth, tenth and fifteenth sessions. Each test was numbered from 1 to 4, respectively.

Mixed ANOVA showed significant main effects both groups, but not with all tests. In enhancement

NF protocol, time has significant main effect on forward digit span (F = 4,452, p = 0,013, and

η2 = 0,358), mental rotation accuracy (F = 4,073, p = 0,018, and η2 = 0,337), and mental rotation

response time (F = 3,667, p = 0,026, and η2 = 0,314); group has significant main effect on backwards

digit span (F = 8,280, p = 0,021, and η2 = 0,509) and mental rotation accuracy (F = 6,181, p = 0,038,

and η2 = 0,436); and group-time interaction has only main effect on mental rotation accuracy

(F = 5,323, p = 0,006, and η2 = 0,400). In suppression NF protocol, time has significant main effect on

mental rotation accuracy (F = 10,423, p < 0,001, and η2 = 0,566); group and group-time interaction has

no effect on any performance assessment.

32

5.2.1. Forward digit span results

In table 2 it is possible to consult the results from each group and protocol and are also

represented in figure 32. The observation of the plots appear to indicate that there is an increment in

results over time in each protocol, except in suppression protocol performed by group 1, in which

seems that there is no change in forward digit test. The most evident results refers to the

enhancement of IAB in group 2.

Table 2: Forward digit span results.

The mean is presented first, and the standard deviation is presented in parentheses.

Enhance IAB Suppress IAB

Test 1 Test 2 Test 3 Test 4 Test 1 Test 2 Test 3 Test 4

Group 1 6,0 (1,67) 5,7 (0,82) 6,5 (1,38) 7,2 (1,17) 6,3 (0,50) 6,5 (0,58) 7,0 (0,82) 6,5 (1,00)

Group 2 7,0 (1,87) 7,0 (2,12) 8,5 (2,08) 9,25 (2,5) 6,5 (1,76) 6,3 (1,51) 7,3 (1,86) 7,2 (1,83)

Both 6,5 (1,75) 6,3 (1,62) 7,3 (1,89) 8,0 (2,00) 6,4 (1,35) 6,4 (1,17) 7,2 (1,48) 6,9 (1,52)

Figure 32: Forward digit span results.

Statistical tests were run to evaluate differences between test 1 and test 4, in each NF protocol,

and between test 4 from the first NF protocol performed and test 4 from the second NF protocol. None

of the tests revealed statistically significant changes.

33

5.2.2. Backward digit span results

The results from backward digit span tests are presented en table 3 and represented graphically in

figure 33. The observation of the plots appear to indicate that there is an increment in results over time

in each protocol, except in suppression protocol performed by group 1, in which seems that there is no

change in forward digit test.

Table 3: Backward digit span results.




Group 1 5,3 (1,75) 5,5 (0,84) 5,5 (0,84) 6,5 (1,38) 6,3 (0,96) 6,3 (0,96) 6,0 (1,15) 6,3 (0,96)

Group 2 6,4 (2,70) 8,6 (3,05) 8,3 (1,90) 8,5 (2,65) 5,3 (1,63) 6,3 (1,73) 7,5 (1,64) 7,1 (1,47)

Both 5,8 (2,18) 6,9 (2,59) 6,6 (1,90) 7,3 (2,11) 5,7 (1,42) 6,3 (1,83) 6,9 (1,60) 6,8 (1,32)

Figure 33: Backward digit span results.

Statistical tests were run to evaluate differences between test 1 and test 4, in each NF protocol,

and between test 4 from the first NF protocol performed and test 4 from the second NF protocol. None

of the tests revealed statistically significant changes.

34

5.2.3. Oddball test results

The results from oddball test is presented in terms of its accuracy, i.e., the number of right

responses (click in the ball when the circle appeared) divided by total number of figures that appeared.

The results are presented in table 4 and represented in figure 34. None of the statistic tests applied

revealed significant differences between assessments.

Table 4: Oddball accuracy results.




Group 1 0,43 (0,14) 0,42 (0,10) 0,42 (0,16) 0,47 (0,67) 0,41 (0,13) 0,52 (0,12) 0,49 (0,11) 0,48 (0,06)

Group 2 0,44 (0,08) 0,49 (0,16) 0,53 (0,07) 0,55 (0,09) 0,45 (0,19) 0,45 (0,14) 0,47 (0,11) 0,48 (0,13)

Both 0,43 (0,11) 0,45 (0,13) 0,46 (0,14) 0,5 (0,08) 0,44 (0,16) 0,48 (0,13) 0,47 (0,11) 0,48 (0,10)

Figure 34: Oddball results.

35

5.2.4. Mental Rotation results

The results of mental rotation test are presented in terms of its accuracy, i.e., the number of right

responses divided by the number total of trials. The results are presented in table 5 and graphically

represented in figure 35.

Table 5: Mental rotation accuracy results.




Group 1 0,59 (0,22) 0,73 (0,19) 0,82 (0,15) 0,9 (0,06) 0,88 (0,17) 0,9 (0,11) 0,96 (0,03) 0,98 (0,03)

Group 2 0,93 (0,08) 0,97 (0,04) 0,95 (0,07) 0,91 (0,08) 0,6 (0,22) 0,77 (0,24) 0,87 (0,20) 0,88 (0,17)

Both 0,74 (0,24) 0,84 (0,19) 0,87 (0,14) 0,91 (0,06) 0,71 (0,19) 0,82 (0,20) 0,91 (0,16) 0,92 (0,14)

Figure 35: Mental rotation accuracy results.

Both groups presented significant increase in mental rotation accuracy in the first protocol

executed. In group 1 it was enhancement protocol (t(5) = 4,429, p = 0,007) and in group 2 it was

suppression protocol (Z = 2,232, p = 0,026). There was no statistically significant differences between

test 1 and 4 in opposite direction NF, nor in the interval between protocols.

36

Another data obtained in this test was the time necessary to answer correctly, i.e. response time.

The results are presented in table 6 and graphically represented in figure 36.

Table 6: Mental rotation response time results.




Group 1 4,40 (1,02) 4,28 (1,06) 3,81 (1,02) 3,67 (0,87) 3,50 (0,99) 2,91 (0,89) 3,01 (0,72) 2,96 (0,77)

Group 2 3,17 (0,90) 2,82 (0,39) 2,88 (0,70) 2,77 (0,37) 3,91 (1,25) 3,64 (0,68) 3,58 (0,89) 3,40 (0,95)

Both 3,84 (1,12) 3,61 (1,09) 3,44 (0,98) 3,31 (0,83) 3,75 (1,11) 3,35 (0,81) 3,35 0,84) 3,32 (0,87)

Figure 36: Mental rotation response time results.

Although both groups apparently decrease the response time in all protocols, only group 1 had

statically significant reduces response time (t(5) = 3,802, p = 0,013). Whilst in the second protocol,

there were no significant differences in the tests. The interval between protocols do not present any

significant difference in any group.

37

5.2.5. MHI-5 results

The final assessment was MHI-5. Table 7 presents the results in both groups and protocols, and its

graphical representation can be observed in figure 37. None of the statistic tests revealed a significant

difference over sessions or between sessions.

Table 7: MHI-5 results.




Group 1 23,7 (2,58) 22,0 (2,68) 22,2 (3,43) 24,0 (1,41) 24,0 (2,58) 23,5 (3,11) 23,8 (2,22) 23,0 (2,94)

Group 2 23,2 (3,96) 23,0 (3,96) 24,0 (2,71) 25,0 (2,27) 21,3 (4,18) 22,3 (2,58) 22,2 (2,14) 22,3 (2,25)

Both 23,5 (3,11) 22,5 (2,95) 22,9 (3,14) 24,4 (1,27) 22,4 (3,72) 22,8 (2,70) 22,8 (2,20) 22,6 (2,41)

Figure 37: MHI-5 response time results.

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6. Discussion

This section aims to explore the results presented in the previous chapter. The first subchapter is

dedicated to the EEG results while the second subchapter is dedicated to the results of the tests.

6.1. EEG results

The first information to stress from the results is the ability that both groups present to modify their

IAB relative amplitude accordingly to the direction defined in each NF training. In other words, if the

objective of NF training was to up-regulate IAB relative amplitude, both groups were able to increment

their IAB relative amplitude during the training and over sessions. In the opposite NF training was also

true.

The first protocol performed by the groups, either enhancement in group 1 or suppression in group

2, had similar correlation between IAB relative amplitude and sessions, r = 0,614 in group 1 and r = -

0,639.

A careful observation of the second protocol that each group performed reveals different

correlations. The correlation in enhancement NF protocol in both groups can reveal that the correlation

between IAB relative amplitude and sessions is higher in group 2 (r = 0,922) comparing to group 1

(r = 0,614). The difference between the two groups was that group 1 had no previous NF experience

when executed that protocol, while group 2 had performed the suppression protocol previously. This

could indicate that suppression NF can facilitate the enhancement NF.

Notwithstanding, group 1, that performed suppression NF after the enhancement NF, had only a

moderate correlation and was not statistically significant (r =-0,393, p = 0,148). It should be referred

that the four elements that completed the second protocol this group had reported excessive during

NF training.

One curious result refers to the baseline, in particular EO. Not only when executing enhancement

protocol but also during the suppressing protocol, it was verified a positive trend. However the strong

correlation is only observed in the first NF protocol executed by each group. It is unclear the reason for

these results.

6.2. Assessment tests

The first test applied was digit span, which is a commonly used test to evaluate the short-term and

working memory. The results in this study did not find any significant effect in any variant of the test.

This was one of the tests that was expected to reveal improvements, at least with enhancement NF

39

protocol due to previous works found in the literature (Escolano et al., 2011; Nan et al., 2012). The

reason why these results differ from the literature could be due to methodological difference.

The next test evaluated was oddball, which did not presented any significant difference after NF

training. Another assessment that did not presented differences during NF protocols was MHI-5.

Relatively to the mental rotation, some differences were found. Mental rotation accuracy in the first

protocol performed by each group presented a significant increase – in group 1 it was the protocol to

enhance IAB amplitude while in group 2 it was the protocol to suppress IAB amplitude. This results

does not associate one direction of NF to this improvement in mental rotation. Nonetheless, group 1

presented a decrease of response times in the first protocol.

When the subjects train their IAB in the opposite direction there was no significant differenced,

which suggests that the gains obtained were maintained in group 1, but there was no improvement in

enhancement NF of group 2.

Another relevant remark from the test results is that there was no significant differences between

protocols, suggesting that the gains in mental rotation were also maintained during the interval

between protocols.

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7. Conclusions and future work

This is the last chapter of this dissertation and is dedicated to present the conclusions and

limitations of this study. It is also proposed future work in order to overcome those limitations.

7.1. Conclusions

This study revealed that it was possible to successfully up- and down-regulate IAB relative

amplitude matching up with NF training performed. The cognitive performance improvements in the

first protocol that each group performed were maintained not only one month after the last session, but

they were not disturbed in the opposite protocol.

In general, the objectives of this work were achieved, revealing that it is possible to alter

consciously the brain waves through NF with success and the gains did not change over time nor with

the NF in the opposite direction.

7.2. Limitations and future work

The biggest limitation to stress is the reduced number of subjects that concluded the experiment.

Each group had initially six elements, which could be sufficient in a pilot study. However, two subject

from each group dropped out. This low number of elements also limits the statistical analysis. Most

studies had drop outs, however, NF is time-consuming which makes recruitment and adhesion harder.

One of the future works suggested is to recruit more volunteers, which is already in progress, and

proceed with the collection of more data.

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9. Annexes

9.1. Brain regions and associated functions

Table 8: Brain regions, location and associated functions, problems and considerations.

Adapted from (Demos, 2005).

Region Site Functions Problems and considerations

Frontal lobes FP1, FP2, FPZ, FZ, F3,F4, F7, F8

Left hemisphere: working memory, concentration, executive planning, positive emotions.Right hemisphere: episodic memory, social awareness.Frontal poles: attention judgment.

Left hemisphere: depression.Right hemisphere: anxiety, fear, poor executive functioning.

Sensorimotor cortex

CZ, C3, C4 Left hemisphere: attention, mental processing.Right hemisphere: calmness, emotion,empathy.Combined: fine motor skills, manualdexterity, sensory and motor integration and processing.

Paralysis (in stroke), seizure disorder, poor handwriting, Attention Deficit Hyperactivity Disorder symptoms.

Temporal lobes T3, T4, T5, T6 Left hemisphere: word recognition, reading, language, memory.Right hemisphere: object recognition, music, social cues.Facial recognition.

Anger, rage, dyslexia, long-term memory, closed head injury.

Parietal lobes Pz, P3, P4 Left hemisphere: problem solving, math, complex grammar, attention, association.Right hemisphere: spatial awareness, geometry.

Dyscalculia sense of direction learning disorders.

Occipital lobes OZ, O1, O2 Visual learning, reading, occipito-parieto-temporal functions.

Learning disorders.

Cingulate gyrus FPZ, FZ, CZ, PZ, OZ Mental flexibility, cooperation, attention, motivation, morals.

Obsessions, compulsions, tics, perfectionism, worry, Attention Deficit Hyperactivity Disorder symptoms, Obsessive CompulsiveDisorder and Obsessive Compulsive Disorder spectrum.

Broca’s area F7, T3 Verbal expression. Dyslexia, poor spelling, poor reading or verbal comprehension.

Wernicke’s area

Parieto-temporal junction

Verbal-understanding.

Left hemisphere

All odd numbered electrodes

Logical sequencing, detail oriented, language abilities, word retrieval, fluency, reading, math, science, problem solving, verbal memory.

Depression (underactivation).

Right hemisphere

All even numberedsites

Episodic memory encoding, social awareness, eye contact, music, humor, empathy, spatial awareness, art, insight, intuition, non-verbal memory, seeing the whole picture

Anxiety (overactivation).

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9.2. Informed consent

Informed Consent for NF training

Subject code: NF_________

Information:

Nature of the Work

The neurofeedback training is a pure Scientific Research project.

Participants Institutions

Joint project between the Evolutionary Systems and Biomedical Engineering Lab of System and Robotics Institute-Lisbon(LaSEEB-ISR-IST) and the Biomedical Engineering Lab of University of Macao (UM-BME).

Objectives

The aim of the project is to explore the dynamic range of neurofeedback by enhancing and suppression of the sameelectroencephalographic brain frequency band.

Procedure during recording sessions

There are two groups: group of enhancement-suppression, group of suppression-enhancement. The group of enhancement-suppression will perform 15 sessions of neurofeedback to increase alpha at Cz, and then another 15 sessions to decreasealpha at the same localization. The group of suppression-enhancement will perform 15 sessions of neurofeedback to decreasealpha at Cz, and then another 15 sessions to increase alpha at the same localization.

The subject sits comfortably on a chair facing a computer screen, where the feedback information (in a form of variable size balland a moving cube) is provided. An electroencephalography (EEG) cap with 20-channel silver-silver chloride (Ag-AgCl)electrodes will be glued with the help of a conductive saline hypo-allergic gel and three additional surface electrodes will gluedto the back of the ears (M1,2) and on forehead (ground electrode).

Before the first session and every 5 sessions, besides the training session, the subject performs evaluation to assess the effectsof neurofeedback training in short term memory, working memory, attention, and mental rotation ability. It also will be performeda mental health inquiry. Before and after each session, the subject is asked to stay quiet with eyes open, and eyes closed for 2minutes. During all sessions, the subject is asked to perform cognitive thoughts in order to increase the size of the feedbackball, better still to move a cube icon upward.

Warnings

Subjects not suitable for this project: pregnancy state, using any sort of chronic medication or additive drugs (legal or illegal),suffering from any kind of Neurologic, Psychiatric or Psychological disorder and minor of age (less than 18 years).

Side Effects

Based on several hundred papers of neurofeedback, no side effects for normal subjects have been reported so far.

Confidentiality

All data are maintained anonymously and used exclusively for research purpose only. Subjects are entitled to inspect their ownrecordings. Subjects are free to be removed from the project anytime without needs of justification and without anyconsequences.

I accept to participate in this project and declares that I am fully informed and understood the experiments performedand do not belong to the warning group defined in this form.

Printed Complete Name: __________________________________________________

Date: Lisbon, ____ /____ / 2016

Signature: ______________________________________________________________

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9.3. MHI-5

INVENTÁRIO DE SAÚDE MENTAL (MHI-5)

Abaixo vai encontrar um conjunto de questões acerca do modo como se sente no dia a dia. Respondaa cada uma delas assinalando num dos quadrados por baixo a resposta que melhor se aplica a si.

1. Durante quanto tempo, no mês passado se sentiu muito nervoso?

⃣ Sempre (1 ponto)⃣ Quase sempre (2 pontos)⃣ A maior parte do tempo (3 pontos)⃣ Durante algum tempo (4 pontos)⃣ Quase nunca (5 pontos)⃣ Nunca (6 pontos)

2. Durante quanto tempo, no mês que passou, se sentiu calmo e em paz?

⃣ Sempre (6 pontos)

⃣ Quase sempre (5 pontos)⃣ A maior parte do tempo (4 pontos)⃣ Durante algum tempo (3 pontos)⃣ Quase nunca (2 pontos)⃣ Nunca (1 pontos)

3. Durante quanto tempo, no mês que passou, se sentiu triste e em baixo?

⃣ Sempre (1 ponto)⃣ Quase sempre (2 pontos)⃣ A maior parte do tempo (3 pontos)⃣ Durante algum tempo (4 pontos)⃣ Quase nunca (5 pontos)⃣ Nunca (6 pontos)

4. Durante quanto tempo, durante o mês que passou, se sentiu triste e em baixo, de tal modo que nada o conseguia animar?

⃣ Sempre (1 ponto)⃣ Com muita frequência (2 pontos)

⃣ Frequentemente (3 pontos)

⃣ Com pouca frequência (4 pontos)⃣ Quase nunca (5 pontos)⃣ Nunca (6 pontos)

5. No último mês durante quanto tempo se sentiu uma pessoa feliz?

⃣ Sempre (6 pontos)⃣ Quase sempre (5 pontos)

⃣ A maior parte do tempo (4 pontos)

⃣ Durante algum tempo (3 pontos)⃣ Quase nunca (2 pontos)⃣ Nunca (1 ponto)

47

Documents

Dynamic Range of Neurofeedback - ULisboa · (Fernado Pessoa) in Livro do Desassossego iii. iv. Abstract Neurofeedback (NF) is an operant conditioning that allows subjects to control