Aves Trnasfer

Avian visual perception:

Interocular and intraocular transfer

and

head-bobbing behaviour in birds

A Dissertation submitted for

the Degree of Philosphiae doctoris (PhD) in Neuroscience

at the

International Graduate School of Neuroscience (IGSN)

of the

RUHR-UNIVERSITY BOCHUM

by

Laura Jimnez Ortega

October 2005

Printed with permission of the International Graduate School of Neuroscience of the RUHR-UNIVERSITY BOCHUM First Referee: Prof. Dr. Nikolaus F. Troje Second Referee: Prof. Dr. Onur Gntrkn Third Referee: Prof. Dr. L. Huber (Wien) Date of the oral examination: 30-11-2005

Table of contents

1. GENERAL INTRODUCTION....................................................................................1

1.2 Intraocular and interocular transfer in pigeons ............................................................................................... 2 1.2.1 Intraocular transfer of information ......................................................................................................... 3 1.2.2 Interocular transfer of information.......................................................................................................... 5 1.2.3 Interim summary ....................................................................................................................................... 9

1.3 Visual asymmetries in birds.............................................................................................................................. 10 1.3.1 Right eye/left hemisphere dominances ................................................................................................... 11 1.3.2 Left eye/right hemisphere dominances .................................................................................................. 12 1.3.3 Asymmetric interhemispheric transfer .................................................................................................. 14 1.3.4 Interim summary ..................................................................................................................................... 16

1.4 Head-bobbing in birds ...................................................................................................................................... 16 1.4.1 Biomechanical function ........................................................................................................................... 17 1.4.2 Image stabilization ................................................................................................................................... 18 1.4.3 Motion parallax........................................................................................................................................ 19 1.4.4 Head-bobbing birds ................................................................................................................................. 20 1.4.5 Interim summary ..................................................................................................................................... 22

1.5 Anatomical substrate ........................................................................................................................................ 22 1.5.1 The avian eye............................................................................................................................................ 22 1.5.2 Visual pathways in the avian brain ........................................................................................................ 26 1.5.3 Interim summary ..................................................................................................................................... 30

1.6 Goals of this work ............................................................................................................................................. 31

2. GENERAL METHODS ...........................................................................................32

2.1 Experimental arena .......................................................................................................................................... 32

2.2 Motion capture system ...................................................................................................................................... 33

2.3 Subjects ............................................................................................................................................................. 34

2.4 Training Procedure .......................................................................................................................................... 34

3. EXPERIMENT 1, 2 AND 3: INTRAOCULAR AND INTEROCULAR TRANSFER IN PIGEONS. ..................................................................................................................38

3.1 Experiment 1: Limits of intraocular transfer in pigeons I: frontal to lateral direction. ................................ 38 3.1.1 Methods .................................................................................................................................................... 39 3.1.2 Results....................................................................................................................................................... 41 3.1.3 Discussion ................................................................................................................................................. 46

3.2 Are pigeons capable of interocular transfer between the two yellow fields? .................................................. 49 3.2.1 Methods .................................................................................................................................................... 50

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3.2.2 Results....................................................................................................................................................... 51 3.2.3 Discussion ................................................................................................................................................. 53

3.3 Limits of intraocular transfer in pigeons II: lateral to frontal direction. ....................................................... 56 3.3.1 Methods .................................................................................................................................................... 56 3.3.2 Results....................................................................................................................................................... 57 3.3.3 Discussion ................................................................................................................................................. 59

3.4 Interim summary............................................................................................................................................. 62

4. EXPERIMENT 4: PATTERN RECOGNITION DURING HEAD-BOBBING: ARE PIGEONS CAPABLE OF PATTERN RECOGNITION DURING THE THRUST PHASE? .....................................................................................................................63

4.1 Methods............................................................................................................................................................. 63

4.2 Results ............................................................................................................................................................... 67 4.2.1 Percentage of correct responses.............................................................................................................. 67 4.2.2 Head-bobbing motion .............................................................................................................................. 69 4.3.3 Interim summary ..................................................................................................................................... 81

5. EXPERIMENT 5: WHY DO BIRDS BOB THEIR HEADS? ....................................82

5.1 Methods............................................................................................................................................................. 83 5.1.1 List of head-bobbing and non head-bobbing birds ............................................................................... 83 5.1.2 Taxonomic tree of head-bobbing and non head-bobbing birds ........................................................... 85 5.1.3 Analysis of behavioural and ecological factors under head-bobbing .................................................. 87

5.2 Results ............................................................................................................................................................... 89 5.2.1 Head-bobbing and non head-bobbing birds list .................................................................................... 89

5.3 Discussion ....................................................................................................................................................... 100 5.3.1 List of head-bobbing and non-bobbing birds: exceptions within a family........................................ 101 5.3.2 Rare or occasional head-bobbing behaviour ....................................................................................... 103 5.3.3 Are body-bobbing birds head-bobbing birds? .................................................................................... 106 5.3.4 Are other-head-movements functions similar to head-bobbing functions? ...................................... 106 5.3.5 Head-bobbing evolution ........................................................................................................................ 107 5.3.6 Ecological and behavioural factors under head-bobbing, body-bobbing and non-bobbing ........... 114 5.3.7 Interim Summary .................................................................................................................................. 115

6. GENERAL DISCUSSION .....................................................................................117

6.1 Intraocular and interocular transfer of information.................................................................................... 117 6.1.1 Intraocular transfer of information ..................................................................................................... 118 6.1.2 Interocular transfer of information...................................................................................................... 120

6.2 Pattern recognition during head-bobbing...................................................................................................... 122

6.3 Why do birds bob their heads? ....................................................................................................................... 124

6.4 Summary ......................................................................................................................................................... 126

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APPENDIX................................................................................................................128

A. Intraocular and interocular transfer ............................................................................................................ 128

B. Pattern recognition during head-bobbing ................................................................................................... 132

C. Why birds bob their heads?........................................................................................................................... 134

REFERENCES .........................................................................................................157

iv

ABSTRACT

Two aspects of the avian visual perception were investigated: inter- and intraocular transfer of

information in walking pigeons as well as head-bobbing behaviour in birds. The retina of the

pigeon has two areas of enhanced vision: the red field pointing into the frontal binocular field

and the yellow field projecting into the lateral monocular field. The entire retina projects to the

tectofugal pathway, whereas the monocular area projects to the thalamofugal pathway. The

first part of this study examines how information received in different retinal areas is

generalised in the pigeon brain. The pigeons task was to discriminate between two shapes by

pecking on one of the two keys located at one end of an experimental alley, while walking

between two feeders. In the first study intraocular transfer between the red and the yellow field

was tested, by moving the stimulus presentation from the frontal to the lateral visual field in

consecutive steps. When the stimuli were located at 45 in the experimental arena, we observed

a drastic decrease of performance that may be due to a switch between the tectofugal and the

thalamofugal pathway. Intraocular transfer of information was also tested from lateral to

frontal direction. The transfer of information was poor or inexistent. Interocular transfer of

information between the yellow fields of the eyes was also tested. A lack of interocular transfer

was found in eight out of nine birds. Pigeons showed more difficulties to learn the task in the

monocular right visual field than in the monocular left visual field.

It is widely accepted that head-bobbing (HB) may act as an optokinetic behaviour, stabilizing

the retinal image and allowing pattern recognition during the hold phase. Pattern discrimination

during HB was tested by presenting two shapes during the hold phase, the thrust phase, or

randomly. The pigeons discriminated the shapes during the entire HB cycle: no differences

between the phases were observed. Finally, a list of 322 species of head-bobbing and non-

bobbing birds is offered. The development of HB in evolution and its behavioural and

ecological characteristics were also investigated. Half of the birds of the world may be head-

bobbing birds; the rest may be equally divided between body-bobbing (hopping) and non-

bobbing birds. HB may have appeared for the first time in a common ancestor of all living

birds. However, evidence for suppressions and several independent evolutions of HB were

observed. Head-bobbing may be a mechanism developed early in evolution to solve visual

demands, like pattern recognition and to monitor predators, in birds with lateralised eyes.

v

General Introduction

1

1. GENERAL INTRODUCTION

Birds are the most visually dependent class of vertebrates (Gntrkn, 2002), as they are

highly specialised in visual perception. They live in a wide variety of habitats from desert to

rain forest and feed on a wide range of food: seeds, insects, small mammals, carcass, etc. Some

birds suffer a strong predator pressure, while others are predators themselves. Birds may need

to afford different visual demands that lead to different visual specialisations. The flying ability

is probably one of the greatest challenges for the avian visual system. For these reasons avian

models have often been used to investigate different aspects of the visual system.

The optic nerves in birds are almost completely decussated (Weidner, Reperant, Miceli, Haby,

& Rio, 1985), furthermore the birds brain has a limited amount of interhemispheric

commissures (Bischof & Watanabe, 1997; Ehrlich & Saleh, 1982; Saleh & Ehrlich, 1984) and

a lack of corpus callosum. Due to these unique characteristics, cerebral asymmetries, using the

avian visual model, have been broadly investigated. These asymmetries represent an important

neural principle in many vertebrates brains, including humans (Rogers & Andrew, 2002).

There is much evidence indicating that interhemispheric interactions may be an important

component for understanding visual asymmetries (Gntrkn & Bohringer, 1987; Keysers,

Diekamp, & Gntrkn, 2000; Parsons & Rogers, 1993). In this context, the study of

interocular transfer and intraocular transfer of information in the avian brain may also

contribute to a better understanding of visual asymmetries in vertebrates.

Many studies about asymmetries have been done in chickens and pigeons (Gntrkn, 1997a).

As a result, we have a better understanding of the visual system of those animals (Zeigler &

Bischof, 1993), although there are still many unresolved questions. One open question is the

role of head-bobbing in visual perception. Pigeons and chickens are head-bobbing birds, that

is, they move the head backward and forward while walking and landing (Dagg, 1977b;

Dunlap & Mowrer, 1930).


2

Head-bobbing is present in at least 40% of the birds, furthermore it has been demonstrated that

head-bobbing is controlled visually (Friedman, 1975b).The head-bobbing function is not yet

well understood, however the contribution of head-bobbing in visual perception is widely

accepted (Davies & Green, 1988; Friedman, 1975; Green, Davies, & Thorpe, 1992; Green,

Davies, & Thorpe, 1994; Troje & Frost, 1999, 2000).

Very often in inter- and intraocular transfer studies, the possible role of optic flow and head-

bobbing in visual perception was not considered. In most cases, the experimental conditions of

the studies prevent the birds to show head-bobbing (examples can be found in: Mallin &

Delius, 1983 ; Nye, 1973; Remy & Emmerton, 1991b; Roberts, Phelps, Macuda, Brodbeck, &

Russ, 1996). In addition, there are few experiments investigating interocular transfer between

the yellow visual fields. This is probably due to the difficulties in training pigeons to solve

visual tasks in the lateral visual field (Remy & Watanabe, 1993).

The main aim of this work is to combine these two aspects of the visuals system in birds: on

the one hand to contribute to a better understanding of information transfer and its

asymmetries, and on the other hand to investigate the functional significance of head-bobbing

in birds.

1.2 Intraocular and interocular transfer in pigeons

Pigeons and many other birds have lateralised eyes. The Pigeons eye is specialised to acute

near binocular vision at short distances during pecking and to panoramic vision at long

distances (Bloch & Martinoya, 1982a; Goodale, 1983). These two different visual functions are

mediated by two separate visual fields that project into two retinal areas: a binocular dorso-

temporal red field and a monocular yellow field. The red field is pointing into the lower visual

field, while the yellow field is pointing into the upper frontal and lateral visual fields.

In a natural situation a bird might perceive stimuli with both eyes, and also with different areas

of the retina. The main goal of inter- and intraocular transfer experiments is to clarify the way


3

in which information retrieved from both eyes and different retinal areas is integrated in birds

brains (Remy & Watanabe, 1993).

1.2.1 Intraocular transfer of information

Intraocular transfer experiments in birds are infrequent and difficult to interpret (Remy &

Watanabe, 1993). Two main limiting factors are responsible for that: first it is difficult to

establish the retinal area in which the stimuli are presented in freely moving subjects; second

training birds in the lateral visual field has been proved to be an arduous task.

The first attempt to train birds in the lateral visual field was done by Nye (1973). He trained six

pigeons in 4 different tasks: rectangular bar detection task, rotating disk of bars detection

task, colour (red and green) and brightness (high and low) discrimination tasks. Birds learned

the task successfully when the stimuli were presented behind the pecking keys in the frontal

visual field. In contrast, when the stimuli were presented laterally in screens located 90 to each

side of the axis of the beak, the response of the birds dropped to chance level. Further attempts

to train the birds with stimuli presented in the lateral screens did not succeed. The pigeons

performed at chance level after weeks of training in the bar and rotating disk detection

tasks. For colour and brightness discrimination the author trained the pigeons initially in the

frontal visual field and moved the screens in 18 azimuth steps to the lateral sides. A

progressive drop of percentage of correct responses to chance level occurred when approaching

90. Nye concluded that pigeons do not possess the neural capability required to learn to use

information contained in laterally located stimuli to directly control pecking behaviour.

In a previous experiment, Levine (1952) found a drop in the discrimination performance when

the stimuli were shifted from a subrostral to an anterorostral position. He interpreted these data

as a lack of intraocular transfer in pigeons between two separate functionally independent

retinal areas.


4

Mallin and Delius (1983) conducted an intraocular transfer experiment in head fixed pigeons.

The birds were trained to discriminate two coloured lights using jaw movements

(mandibulando) as an operant response. They found a weak transfer of light colour

discrimination from one locus to another within the visual field of the same eye. Interestingly,

they also found a poor intraocular discrimination transfer of coloured lights when the stimuli

were shifted from frontal to lateral position and vice versa. However, the transfer from lateral

to frontal position was slightly better (around 10%) than the reverse performance. These

observations were confirmed by Remy and Emmerton (1991b) in head-fixed pigeons, who

described the existence of information transfer from the lateral to frontal visual field and

observed a lack of information transfer from the frontal to the lateral visual field in a light

discrimination task.

Most recently, Roberts et al. (1996) trained eight unrestrained pigeons in an experimental

chamber to perform a symbolic delayed matching to sample task. The results confirm previous

findings obtained in head-fixed pigeons (Mallin & Delius, 1983; Remy & Emmerton, 1991b),

that is, there is intraocular transfer of information from the lateral to the frontal visual field, but

not vice versa. They also demonstrated that pigeons are capable of discriminating stimuli in the

lateral visual field, in contradiction to Nyes hypothesis (1973).

Two main suggestions have been proposed to explain intraocular transfer asymmetries. First,

Nye (1973) argued that pigeons were incapable of learning a discrimination task that requires a

pecking response when the stimuli are presented in the lateral visual field. However, it has

been demonstrated that pigeons are capable of stimulus discrimination in the lateral visual field

(Bloch & Martinoya, 1982b; Goodale & Graves, 1982; Mallin & Delius, 1983; Remy &

Emmerton, 1991b; Roberts et al., 1996). Second, it has been proposed that intraocular transfer

of information from the lateral to the frontal visual field may be an ecological advance. On the

one hand, birds should be able to switch from lateral to frontal vision when perceiving food

and approaching to peck (Friedman, 1975; Remy & Emmerton, 1991b; Roberts et al., 1996). In

addition, intraocular transfer from lateral to frontal visual field may be required to monitor the

environment for approaching predators while the frontal vision is occupied in feeding (Remy &

Emmerton, 1991b; Roberts et al., 1996). On the other hand, there is no need for information


5

transfer from the frontal to the lateral field. Usually objects processed by the lateral visual field

are not seen in the frontal field first (Roberts et al., 1996). Field observations suggest that if an

object is processed by the lateral visual field, it is often shifted to the frontal visual field but

rarely vive versa.

1.2.2 Interocular transfer of information

Interocular transfer has been traditionally studied by covering one eye during the process of

learning a visual task. Once the bird reaches a certain criterion of performance, the naive eye

is tested in the same task (Goodale & Graves, 1982).

According to Levine (1945a), the earliest interocular transfer experiment was done in 1917 by

Khler. He observed that chickens showed interocular transfer in discriminating two sheets of

grey paper differing in brightness, which were located horizontally at ground level. In contrast

to Khlers findings, a lack of interocular transfer was found in pigeons trained monocularly in

a go/no-go colour discrimination task. In this experiment the stimuli were displayed on a

vertical screen above ground level (Beritov & Chichinadse, 1935).

Levine conducted a set of experiments using a jumping stand in which birds were placed in a

rotating perch that forced them to jump onto one of two platform according to different stimuli

(colours and shapes discrimination) (Levine, 1945a, 1945b, 1952). If the bird chose the

incorrect platform according to the presented stimuli, it collapsed and the animals dropped into

a net. If the correct platform was chosen, the birds were allowed to stay there for 15 seconds.

He observed that information transfer between the two eyes in pigeons depends on the location

of the stimuli in the visual field with reference to the position of the birds head. If the stimuli

were presented horizontally in a plane below the pigeons head (subrostral), interocular transfer

was present. In contrast, if the stimuli were presented vertically in front of the pigeons head

(anterostral) there was an absence of transfer (Levine, 1945a, 1945b, 1952). Two hypotheses

were proposed to explain these results: the sensorimotor integration hypothesis ( Watanabe,


6

1986) and the retinal locus hypothesis (Goodale & Graves, 1982; Levine, 1945b; Mallin &

Delius, 1983).

The sensorimotor integration hypothesis proposes that pigeons may transfer information

depending on whether the response (manipulandum) and the stimuli (stimulandum) have

the same or different spatial locations. When manipulandum and stimulandum share the same

spatial locations, for example the stimulus is presented on the surface of the pecking key,

interocular transfer of information is expected. If they are located in different spatial location a

lack of interocular transfer is predicted (Remy & Watanabe, 1993).

To test the sensorimotor integration hypothesis, pigeons were trained in three conditional

spatial tasks employing two pecking keys arranged either vertically or horizontally (Watanabe,

1986). No matter whether the keys were arranged horizontally or vertically, if manipulandum

(response of the pigeon) and stimulandum were located in the same pecking key, there was a

perfect interocular transfer of information. However, if manipulandum and stimulandum were

located in different keys (for example: the stimulus was presented in the lower key and the

pigeons had to peck in the upper key) the pigeons were incapable of interocular transfer.

The retinal locus hypothesis proposes that interocular transfer occurs when the stimuli are

presented in the dorso-temporal part of the retina (red field), but not when the stimuli are

presented in the other parts of the retina (yellow field) (Goodale & Graves, 1982). The first

author supporting this hypothesis was Levine (1952). He proposed that in the pigeons eyes

there are at least two independent visual areas: a retinal locus corresponding to the subrostral

position in the visual field (below the head) and a retinal locus pointing into the anterostral

position (in front of the head) of the visual field. He argued that only the subrostral retinal

locus has the required neural connections which mediate interhemispheric transfer of

information. Furthermore, anterostral-subrostral transfer did not occur within a single eye.

Catania (1965) challenged this hypothesis by training pigeons to peck on a key located in front

of the pigeon head, in brightness, colour and pattern discrimination tasks. The stimuli were

projected either on the frontal key or on one of two lateral screens. Pigeons showed interocular


7

transfer of information in both conditions. Catania offered two explanations for the lack of

interocular transfer in Levines experiments. Pigeons are laterally far-sighted and anteriorly

near sighted. In the jumping stand, the pigeons have to cock their head to one side in order to

observe the stimuli with the lateral visual field. The direction in which the head has to be

cocked depends on the covered-eye, and therefore this change of posture may affect interocular

transfer of information. Moreover, the amount of training may influence interocular transfer: In

Catanias studies the pigeons might have been over-trained in comparison to the pigeons in

Levines experiments (Catania, 1965).

A set of experiments replicating Levines jumping stand were designed to investigate Catanias

postural hypothesis (Goodale & Graves, 1982). Furthermore, the authors conducted several

key-pecking (FR1) discrimination tasks to test training amount and task difficulty as possible

factors in interocular transfer. They claimed that the lack of interocular transfer was a genuine

phenomenon which did not depend on postural habit, amount of training and task complexity.

Furthermore, birds trained binocularly in the jumping stand often showed evidence of learning

with only one eye when tested monocularly. They concluded that: the lack of interocular

transfer found in situations such as the jumping stand is a consequence of the discriminative

stimuli falling within the monocular field. Therefore, Goodale and Graves (1982) proposed

that interocular transfer occurs when the stimuli were projected into the red field, but not when

they were presented to the yellow field

Mallim and Delius (1983) conducted an experiment with head fixed pigeons using jaw

movements (mandibulando) as an operant in a colour discrimination task. They presented two

coloured lights in different locations of the retina. The advantage of this experimental design is

that the spatial localization of the stimuli is separated from the response and the presentation of

the stimuli in a certain retinal locus is controlled. Birds showed interocular transfer of

information when the discrimination task was monocularly presented inside the red field and a

lack of interocular transfer when the stimulus was presented within the yellow field. These

results support the retinal locus hypothesis, although Remy and Watanabe (1993) pointed out

that, in this task, pigeons did not need to direct their response spatially. Furthermore, the


8

pigeons beak was oriented towards the position of the stimuli in the frontal position, whereas

during the lateral stimulation the beak is oriented in a different direction.

The retinal locus and sensorimotor integration hypotheses may not be contradictory.

Retinal locus may be crucial when a task does not require sensorimotor integration. However,

if a task requires sensorimotor integration, interocular transfer will not occur even when the

stimuli falls into the binocular field (Remy & Watanabe, 1993).

In addition, some experimental findings suggest that other characteristics of a task, such as

biological relevance, may influence interocular transfer. A lack of interocular transfer was

found in avoidance of the visual cliff (Zeier, 1970). Transfer of information was absent in heat

reinforcement but it was present in a similar task using food reinforcement (Gaston, 1984).

Interocular transfer was also observed in taste aversion in chicks (Bell & Gibbs, 1979; Gaston,

1984), as well as in cardiac conditioning in pigeons (Mihara & Watanabe, 1982) and in

conditioned withdrawal in pigeons, chickens and gulls (Stevens & Klopfer, 1977).

Furthermore, interocular transfer in pigeons colour discrimination but not in motor response

training has been found (Stevens & Kirsch, 1980). Pigeons eyes were occluded during initial

acquisition of the pecking response and subsequently during learning colour discrimination.

When the animals were tested with the occluded eye they were unable to respond. Once the

pigeons were trained to peck a blank response key, transfer of the colour discrimination task

was observed. This is an interesting result, because most of the pigeons discrimination

experiments involve training of the motor response under binocular condition prior to

monocular training on the experimental task. Additional studies of interocular transfer of the

motor response would be useful to explain this phenomenon (Remy & Watanabe, 1993).

In a recent publication, interhemispheric transfer of memories was tested in pigeons

(Nottelmann, Wohlschlager, & Gntrkn, 2002). Pigeons task was to peck on one of two

vertical keys according to a pattern displayed on both keys. Six pairs of patterns were used, for

half of these pairs the animals had to peck the upper pattern, for the other half the lower one.

Transfer of information from the left eye/right hemisphere to the right eye/left hemisphere, but


9

not vice versa was observed. In this experiment, stimuli are presented within the red field and

sensorimotor integration occurs, however a lack of interocular transfer is found when the

stimuli are presented in the right hemisphere. Therefore, asymmetries in bird brain should be

considered as an important factor for interocular transfer. Most probably, asymmetries and

interocular transfer of information are interrelated phenomena in birds. In fact, Skiba et al

(2000) found asymmetries in interocular transfer of information. A faster shift of learned

colour cues from the dominant right to the left eye than vice versa was reported.

Finally, it should be noted that none of the hypotheses is capable of explaining all experimental

results in interocular transfer. The retinal locus hypothesis together with the current

knowledge of the anatomic aspects and asymmetries will lead to a better understanding of the

interocular transfer phenomenon.

1.2.3 Interim summary

The main goal of inter- and intraocular transfer experiments is to clarify the way in which

information retrieved from both eyes and different retinal areas is integrated in birds brains.

Interocular transfer experiments test the transfer of information between the two eyes (i.e.,

between the two hemispheres), whereas intraocular transfer experiments test the transfer of

information between different retinal areas of the same eye.

Birds have two distinctive retinal areas: a lateral monocular yellow field and a frontal binocular

field, often called the red field. Intraocular transfer has been investigated training the animals

to solve a visual task presented in one of these two visual fields and testing in the other.

Investigations in non walking pigeons have demonstrated that there is information transfer

from the lateral to the frontal visual field. However, a lack of transfer was found from the

frontal to the lateral visual field.

In birds, interocular transfer has been traditionally studied by covering one eye during the

process of learning a visual task. Once the animal reaches a certain criterion of performance,


10

the naive eye is tested in the same task. Interocular transfer depends on the experimental

conditions and the task. Two main hypotheses have been proposed to explain the presence or

absence of interocular transfer: the sensorimotor integration hypothesis and the retinal

locus hypothesis.

The sensorimotor integration hypothesis proposes that pigeons may transfer information if

the response and the stimuli share the same spatial locations. In contrast, if they do not share

the same spatial location, a lack of interocular transfer will be observed. The retinal locus

hypothesis proposes that interocular transfer occurs when the stimuli are presented within the

red field, but not when the stimuli are presented in the yellow field.

1.3 Visual asymmetries in birds

Birds are highly visual animals, their visual capabilities are the most specialised among

vertebrates (Gntrkn, 2003). The optic nerves in birds are almost completely decussated

(Weidner et al., 1985). In addition, the amount of thalamic and mesencephalic commissures in

birds is very limited (Bischof & Watanabe, 1997; Ehrlich & Saleh, 1982; Saleh & Ehrlich,

1984). Consequently, hemispheric asymmetries can be easily investigated by directing the

visual information to one hemisphere by the simple mechanism of temporarily covering one

eye.

These characteristics make the avian visual system a very valuable model for the study of

visual asymmetries. Many studies in visual asymmetries have been done by using a variety of

birds species, like marsh tits (Clayton & Krebs, 1994a), domestic chicks (Andrew, 1988;

Andrew & Dharmaretnam, 1993; McKenzie, Andrew, & Jones, 1998; Rogers & Andrew,

2002, Parsons, 1993 #3354), zebra finches (Alonso, 1998; Voss & Bischof, 2003), European

starlings (Hart, Partridge, & Cuthill, 2000), quails (Valenti, Sovrano, Zucca, & Vallortigara,

2003) and pigeons (Gntrkn & Bohringer, 1987; Gntrkn et al., 2000; Gntrkn &

Hahmann, 1994; Prior & Gntrkn, 2001; Prior et al., 2004; Skiba et al., 2000).


11

1.3.1 Right eye/left hemisphere dominances

Monocular occlusion studies revealed a right eye/left hemisphere dominance in discriminating

two-dimensional artificial patterns in pigeons (Gntrkn, 1985) and three dimensional natural

objects by means of a grain-grit task in pigeons (Gntrkn & Kesch, 1987), zebra finches

(Alonso, 1998) and chickens in a pebble-floor task (Mench & Andrew, 1986). Right eye

system dominance is also found in pattern discrimination (Gntrkn, 1997a). A higher degree

of illusion is observed for the right eye, when the birds were stimulated with geometrical optic

illusions (Gntrkn, 2003).

Some complex studies in pigeons have shown that memories of visual engrams and pattern

information are stored unilaterally in the left hemisphere (Gntrkn, 1997a; Nottelmann et al.,

2002; von Fersen & Gntrkn, 1990). This asymmetry, in memorizing visual stimuli, most

probably results in a right eye/left hemisphere advantage in homing (Ulrich et al., 1999),

although when pigeons are tested in circumstances in which they cannot rely on visual cues,

like landmarks, the left hemisphere advantage vanishes (Prior, Lingenauber, Nitschke, &

Gntrkn, 2002). A right eye dominance is also found in large-scale homing as a consequence

of a strong lateralisation of the avian magnetic compass and optic flow processing in favour of

the left hemisphere (Prior et al., 2004).

There is evidence for left hemisphere asymmetries in cognitive processes such as learning-to-

learn. In a colour discrimination reversal learning task birds learned faster with their right

eye/left hemisphere than with the left eye/right hemisphere (Diekamp, Prior, & Gntrkn,

1999)

Although, it has been demonstrated that the European starling shows an asymmetric

distribution of photoreceptors in the retina, the majority of the asymmetries described are

attributed to genuine central processes. They are not due to peripheral factors such as visual

acuity (Gntrkn & Hahmann, 1994), wavelength discrimination (Remy & Emmerton,

1991a), or depth resolution (Martinoya, Rivaud, & Bloch, 1983).


12

Due to the amount of evidences in favour of the left hemisphere superiority, accumulated early

in the literature, it has been postulated as the dominant hemisphere. At the moment, it is

believed that none of the avian hemispheres dominates completely the visual analysis

(Gntrkn, 2003). In fact, there is also evidence for right hemisphere superiority in a variety

of tasks.

1.3.2 Left eye/right hemisphere dominances

Left eye/right hemisphere dominance has been observed in geometric or spatial information in

marsh tits (Clayton & Krebs, 1994b) and chicks (Tommasi & Vallortigara, 2001; Vallortigara,

2000). A right hemisphere dominance is also found for social recognition, like aggressive and

sexual responding, in chicks (Rogers & Andrew, 2002; Vallortigara, 1992). Wild living

Kookaburras (Dacelo gigas) search for food on the ground using preferably their left eye

(Rogers, 2002). In pigeons, a left eye/right hemisphere advance was found in choice reaction

times to a patter discrimination task (Di Stefano, Kusmic, & Musumeci, 1987). Most recently,

left eye/right hemisphere dominances was observed in the spatial distribution of attention

related to food detection for pigeons and chickens (Diekamp, Regolin, Gntrkn, &

Vallortigara, 2005).

The opposite left-right specialisation hypothesis for the lateral and frontal visual fields propose

that the left eye/right hemisphere may be dominant in the lateral visual field which is mainly

focused at long distances, whereas the right eye/left hemisphere may be dominant in binocular

vision which is specialised on short distance visual processes (Evans & Evans, 1999; Evans,

Evans, & Marier, 1993; Rogers, 2000; Vallortigara, Cozzutti, Tommasi, & Rogers, 2001).

In fact, in the majority of the experiments in visual asymmetries, the stimuli were shown in the

frontal binocular visual field, which is mainly analysed by the tectofugal pathway (Gntrkn

& Hahmann, 1999; Skiba et al., 2000). However, some evidences of lateral visual field

processing have arisen recently. Chickens fixated approaching predators by turning the head


13

abruptly to one side preferably using the left eye (Evans et al., 1993) and showed shorter

reaction times using the left eye to detect a novel moving stimuli (a model raptor) (Rogers,

2000). In contrast, hens responded to a food call by fixating downward with the frontal visual

field. This pattern was not observed when alarm calls and contact calls were presented (Evans

& Evans, 1999). Furthermore, Social recognition experiments showed that chickens use either

the lateral field of its left eye, or the frontal field of the right eye, before pecking at a stranger,

but not at cagemates (Vallortigara et al., 2001).

Having a lateralised brain may allow dual attention to short distance tasks like feeding (using

the right eye/left hemisphere system) and long distance tasks like vigilance for predators (left

eye/right hemisphere system) (Rogers, 2000).

A recent study with pigeons found a left hemisphere dominance of the thalamofugal visual

pathway in a pattern discrimination task in an open arena (Budzynski & Bingman, 2004). The

thalamofugal pathway receives information from the lateral visual field, and therefore it is

assumed that it may be specialised in far field information processing. Therefore, the left

hemisphere dominance in the open arena may contradict the opposite left-right specialisation

hypothesis for the lateral and frontal visual fields in chicks. Moreover, the main asymmetry

was observed in the visual wulst, a structure that belongs to the thalamofugal pathway but also

contributes to the tectofugal pathway (Bagnoli, Grassi, & Magni, 1980; Engelage & Bischof,

1994; Folta, Diekamp, & Gntrkn, 2004; Miceli, Reperant, Villalobos, & Dionne, 1987).

However, it should be taken into consideration that the retinal projection of the stimuli was not

controlled.

Two more alternatives for explaining hemispheric specialisation have been discussed in the

literature. The right eye/ left hemisphere in chicks may be involved in the analysis of novelty

and in the spatial configuration of the environment (R.J. Andrew & Dharmaretnam, 1993).

This proposal is not in contradiction with the opposite left-right specialisation hypothesis for

the lateral and frontal visual fields, indeed a novel stimulus may be perceived first with the

lateral visual field.


14

In addition, asymmetries in the birds visual system may increase the computational speed of

certain processes by concentrating them into one hemisphere. A good example is that visual

lateralisation improves grain-grit discrimination success in pigeons (Gntrkn et al., 2000).

Furthermore in a double task, like finding food and being vigilant for predators, not-lateralised

chicks perform worse than lateralised ones (Rogers, Zucca, & Vallortigara, 2004).

Consequently to the ecological advantages of being capable to attend to both predators and

feeding source, the computational advantages of processing information in one hemisphere

should be added. Most probably the asymmetric avian brain is a consequence of the interaction

between the ecological and computational advantages mediated by the anatomical substrate.

1.3.3 Asymmetric interhemispheric transfer

Various studies have investigated asymmetries of transfer between the two hemispheres. Such

investigations can give valuable cues to understand interhemispheric transfer, visual

asymmetries, and their interactions.

In chickens, a poorer interocular transfer of information from the left eye system to the right

eye system than in the opposite direction was described. A passive avoidance task was used, in

which birds learned to avoid a bead covered with a bitter substance. Binocular and right lesions

in the intermediate hyperstriatum ventrale (IMHV) resulted in amnesia (in monocularly trained

birds) when the chicks were tested with the left eye open. On the other hand, left IMHV lesions

did not impair performance regardless of the eye used (Sandi, Patterson, & Rose, 1993).

Furthermore, lesions in the left IMHV right after training induced amnesia in binocularly

trained birds, whereas bilateral ablations of IMHV lesions made one and six hours post-

training did not result in amnesia (Patterson, Gilbert, & Rose, 1990). Sandi et al (1993)

explained those results as a consequence of a relationship between lateralisation of IMHV

function and the visual asymmetries which occur at the behavioural and structural level. They

proposed a model in which the memory trace is not fixed into the left IMHV, but it is

transferred within one hour to the right IMHV.


15

Another IMHV asymmetry has been found in chicks imprinted with an artificial object. Lesion

studies showed that within the first hours after imprinting there is information transfer from left

IMHV to the right IMHV which may be responsible for storing the visual characteristics of the

imprinted object (Horn, 1991; Nicol, Brown, & Horn, 1995).

An asymmetrical transfer of information has been found in marsh tits for memory storage.

Monocular occlusion was used to investigate lateralisation and memory transfer in a food

storing and in a one-trial associative learning task. In both cases it was found that both eyes are

involved in short-term storage, whereas only the right eye system is responsible for long-term

storage. The results indicated that memories are transferred from the right to the left eye

system between 3 and 24h after the memory formation. Seven hours after the memory

formation, the engram is no longer accessible to the left eye system but has not yet reached the

right eye system (Clayton, 1992; Clayton & Krebs, 1994).

In pigeons, it has been demonstrated that each hemisphere shifts colour information to the

contralateral side, but the efficiency of the transfer is time and side dependent. There is a faster

shift of learned colour cues from the right to the left eye than vice versa within the first 50

minutes after acquisition. For intervals longer than 3 hours, no differences have been found

(Skiba et al., 2000). The authors of this experiment concluded that inter-ocular transfer from

the right to the left eye should be facilitated due to a higher bilateral representation of the left-

sided tectofugal pathway.

The interhemispheric asymmetries in food storing, colour discrimination and passive avoidance

are not in the same directions. Those differences may arise by the diverse types of cognitive

processes required for each task (Skiba et al., 2000). For example, a storing food task demands

the utilization of spatial cues which are mainly processed in the right hemisphere, whereas

visual cues needed for a pattern discrimination task are processed mainly in the left

hemisphere. For giving a coherent explanation of interhemispheric asymmetry patterns, three

factors should be considered, functional asymmetries, time course, and physiological

characteristics.


16


In birds, right eye/left hemisphere dominance is observed in pattern discrimination, stimulus

categorization and memory of visual stimuli. In contrast, left eye/right hemisphere superiority

has been found in processing geometric information, social recognition like aggressive and

sexual responding. It has been recently proposed that the right eye/left hemisphere may be

dominant for short distance tasks like feeding, whereas the left eye/right hemisphere may be

specialised in long distance tasks like vigilance. In addition having an asymmetric brain may

increase computational speed and allow dual attention to short and long distances.

Asymmetries in the information transfer between the two hemispheres have also been

described. In a passive avoidance task a poorer interocular transfer of information from the left

eye system to the right eye system than in the opposite direction was found. In Marsh tits,

memories are transferred from the right to the left eye system between 3 and 24h after the

memory formation. In pigeons, it has been demonstrated that there is a faster shift of learned

colour cues from the right to the left eye than vice versa, within the first 50 minutes after

acquisition.

1.4 Head-bobbing in birds

Pigeons, chickens, moorhens, partridges, storks, crows, ibises, and many other birds show a

characteristic head movement while walking (Dagg, 1977b; Davies & Green, 1988; Dunlap &

Mowrer, 1930; Friedman, 1975; Friedman, 1975; Frost, 1978). In pigeons, the head moves

backward and forward with respect to the body with a frequency that ranges from about 2 to 10

Hz (Troje & Frost, 2000). Head-bobbing is characterized by a hold phase and a thrust phase

(Fig. 2). During the hold phase the head of the bird remains stable in space (Frost, 1978; Troje

& Frost, 2000), whereas during the thrust phase the head is moved forward (Fig. 1 and Fig. 2).

In pigeons, heead-bobbing movement has been observed during walking, landing flight

(Davies & Green, 1991), prior to pecking (Goodale, 1983), and in other behaviours. Even a

stationary bird actively observing its environment, shows head-bobbing behaviour.


17

Head-bobbing was first described in 1930 by Dunlap and Mowrer. Since then, three main

functions have been proposed, a biomechanical function and two visual functions: image

stabilization and depth perception through motion parallax.

Head movement of a walking moorhen

200

400

600

800

1000

1200

1400

0 0.2 0.4 0.6 0.8 1 1.2

Time (s)

Hor

izon

tal d

ispl

acem

ent (

pixe

ls)

1.4

Figure 1: Head position of a walking moorhen (Gallinula chloropus) in freedom. The head position in space was obtained by frame by frame analysis of walking moorhen video recordings. The horizontal coordinate of the head position, given by pixels, was plotted against the time.

1.4.1 Biomechanical function

In walking birds, head-bobbing is synchronized with the motion of the feet (Dagg, 1977a;

Dunlap & Mowrer, 1930). For this reason, the first attributed function to head-bobbing was a

biomechanical function (Dagg, 1977b). However, later it was shown that head-bobbing is

controlled visually and can be elicited independently of active locomotion (Friedman, 1975;

Friedman, 1975; Frost, 1978). Although this finding points clearly to a visual function, head-

bobbing may also have a biomechanical correlation. Body movements are synchronized with

head movements in various behaviours and the stride length of a walking bird is correlated

with the relative magnitude of head-bobbing (Fujita, 2004). Troje and Frost (1999) proposed a


18

central pattern generator involved in coordinating complex motion patterns. Eye stabilization

may play a role in enhancing equilibrium during walking (Fujita, 2002).

1.4.2 Image stabilization

Some remarkable evidences supporting the visual function of head-bobbing were found in

Ring Doves (Friedman, 1975). A single bird was trained to walk inside a cylindrical cage; at

least two of the six experimental conditions demonstrated an unequivocal dissociation between

walking and head-bobbing. In one condition, the bird walked on a mobile false floor while the

cage and the visual surrounding were static. Head-bobbing was not observed in this case. In

another experimental condition, the bird remained static on the floor but the cage was moved

smoothly in a rostral-to-caudal direction, provoking optic flow. A clear head-bobbing

behaviour was observed in this situation. These findings were corroborated in pigeons: head-

bobbing was abolished when the animals walking on a treadmill matched the belt velocity,

confirming that head-bobbing is visually elicited (Frost, 1978).

Taking in account those results, it was suggested that the hold phase could be similar to other

optokinetic behaviours stabilizing the retinal image (Frost, 1978). During the hold phase the

head is not completely stabilized, but it slips slightly providing the necessary error signal that

drives the compensation mechanism to stabilize the head (Frost, 1978; Troje & Frost, 2000).

Stabilizing the retinal image allows object recognition and allows the visual system to

distinguish between self motion and outside world motion (Davies & Green, 1988; Frost, 1978;

Troje & Frost, 1999). Whooping cranes, during foraging, walk at speeds that permit them to

keep their heads immobilized with respect to the visual surroundings while covering large

search areas (Cronin, Kinloch, & Olsen, 2005). In spite of the fact that image stabilization is

widely accepted as a head-bobbing function, it has been found that in running and landing

pigeons the hold phase is replaced with a flexion phase which maintains alternation between

two different head velocities. However, in these cases the retraction of the head does not

compensate the fast forward movement of the body and the head is not stabilized (Green, 1998;


19

Green et al., 1994). These observations suggest that head-bobbing may have several functions

depending on the situations and environmental demands.

1.4.3 Motion parallax

During the thrust phase, pigeons and other birds may use motion parallax computation to

derive distances. Pigeons and many other birds like ibises, storks, partridges, chickens,

woodcocks etc. have laterally placed eyes with very small binocular fields. Stereo vision as a

cue for depth perception can play a role only in a very restricted area. It is therefore assumed

that birds use motion parallax to monocularly derive depth information (Green et al., 1994).

Figure 2: Stroboscopic image from a walking pigeon that illustrates the typical head-bobbing which consists of a period in which the head remains fixed in space (hold phase) and a period in which it is quickly moved forward (thrust phase). From: (Frost, 1978).

S

W

K

&

t

d

f

M

d

everal animal species discriminate depth through motion parallax: locust (Collett, 1978;

allace, 1959), praying mantis (Kral, 1998, 2003; Poteser & Kral, 1995; Poteser, Pabst, &

ral, 1998), barn owl (van der Willigen, Frost, & Wagner, 2002) and gerbils (Goodale, Ellard,

Booth, 1990). Those animals perform head movements called peering in order to generate

he necessary optic flow for motion parallax computation. Bees are also capable of calculating

epth through motion parallax taking advantage of the ambient optic flow generated during

lying (Lehrer, Srinivasan, Zhang, & Horridge, 1988).

otion parallax computation is based on the fact that a translation of the eye induces a

isplacement of the retinal image of an object. The translation of the eye xh and the


20

displacement of the retinal image of an object xr are related by the ratio of the focal length f of the eye and the distance d of the object (Fig. 3).

d fxhxr---------=

Figure 3: Motion parallax computation where d is the distance to the object, f is the focal length, xh is the translation of the eye, and xr is translation of the retinal image.

The displacement of the eye xh and the corresponding shift of the retinal image xr can well

be replaced by the respective velocities vh and vr:

d fvhvr-----=

Whereas f is an anatomical constant and vr can be derived directly from the visual input, the

velocity of the eye with respect to the visual surroundings vh has to be determined independently. In a walking bird this may be achieved by propioceptive and vestibular

information. In praying mantis the propioceptive cervical hair plate sensilla are involved in the

measurement of the distance to a jump target with the aid of motion parallax actively produced

by translatory head motion (Poteser et al., 1998).

1.4.4 Head-bobbing birds

Although head-bobbing behaviour has been very often discussed in the literature, there exists

no comprehensive list about which birds do and which ones do not. Frost (1978) reported that

irds, such as pigeons, doves, hens, head-bobbing occurs in at least 8 of the 27 orders of bstarlings, pheasants, coots, moorhens, rails, sand-pipers, phalaropes, parrots, magpies, and

quails. Dagg (1977) listed 28 head-bobbing and 21 non head-bobbing species during

locomotion. These lists are rather incomplete and some birds could be misclassified, but they


21

suggest that at least 1/3 of the birds could show head-bobbing. Furthermore, the ecological

behavioural and phylogenetic information have been rarely considered in the study of head-

bobbing.

To our knowledge, apart from these reports there is a lack of information in the literature about

head-bobbing birds. Most of the articles focus on pigeons head-bobbing behaviour without

retrieving data about other species that could help to clarify its functional significance.

An unanswered question is why some birds bob their heads, whereas other birds walk without

bobbing their heads. Furthermore, it is not a clear answer why some species of birds walk with

or without displaying head-bobbing. Some birds like magpies can walk with head-bobbing, run

or hop. Head-bobbing during walking is used for low velocities, whereas running and out-of-

phase hopping are alternative gaits for higher speed in magpies. Furthermore, it is not known

why some birds use running and hopping as alternative gaits and why they prefer hopping over

running at high speeds (Verstappen, Aerts, & Van Damme, 2000).

Dagg (1977) reported that Mynah birds and starlings alternated between walking with head-

bobbing and hopping, depending on the speed of the motion. Birds that walk and bob their

heads tend to be of intermediate size. Small birds like most of the Passeriformes, living in

bushes and trees, with short legs tend to hop rather than walk (Friedman, 1975).

Hopping behaviour in birds may be comparable to head-bobbing and may play a similar role

(Davies & Green, 1988; Friedman, 1975). A frame by frame analysis of hopping sparrows

(Passer domesticus) while foraging reveals that birds head is thrust forward before the legs

start to push the body into the air. Likewise, the head stops and is stabilized in the visual space

before the body finished landing from the hop. This behaviour is also observed in alert

sparrows but not in somnolent ones (Friedman, 1975).


22


Many birds show a characteristic forward and backward head movement while walking,

running, and during landing flight called head-bobbing. It is characterized by a hold phase and

a thrust phase. Typically, during the hold phase the head of the bird remains stable in space

while during the thrust phase the head is moved forward. Three main functions for head-

bobbing have been proposed: biomechanical function, image stabilization, and depth

perception through motion parallax. Although head-bobbing behaviour has been very often

discussed in the literature, most of the birds that bob their heads are not listed. Dagg (1977) and

Frost (1978) reported that head-bobbing occurs in at least 8 of the 27 orders of birds and in 28

species such as pigeons, doves, hens, starlings, pheasants, etc. It has been proposed that

hopping in birds could be comparable to head-bobbing. It is not known why head-bobbing

occurs in some species of birds but not in others. Further investigations are required to

investigate the functional and ecological significance of head-bobbing behaviour.

1.5 Anatomical substrate

The avian visual system is composed of two parallel visual pathways that process retinal

information from different parts of the retina: the thalamofugal and the tectofugal pathway. In

addition the accessory optic system is dedicated to the analysis of optic flow. A comprehensive

understanding of the three pathways is important for any attempt to understand the mechanisms

underlying visual asymmetries, inter- and intraocular transfer of information, and head

bobbing.

1.5.1 The avian eye

Birds have large eyes relative to their body size, suggesting that vision is an important sensory

modality in the class aves (Garamszegi, Moller, & Erritzoe, 2002; Martin, 1993). The small

tawny owl (450g) has eyes with a greater axial length than humans. The diameter of the ostrich


23

eye is considered to be amongst the largest of all terrestrial vertebrates, with an axial length

close to 40 mm (Martin, 1993; Martin, Ashash, & Katzir, 2001). The resolution power of the

eye does not depend entirely on its size, other important factors like the structure and

concentration of rods and cones on the retina should be considered. Diverse evolutionary

demands, as diurnal or nocturnal activity, result into different kind of eyes that vary in the

absolute size, position, and amplitude of movement (Martin 1993).

Th avian retina like the mammals retina consist on by five layers: the outer nuclear and

pl

lay

an

sy

co

Th

bl

ox

lik

ce

ob

m

(6

an

eexiform layers, the inner nuclear and plexiform layers, and the ganglion cell layer. These

ers contain five kinds of cells: photoreceptors, bipolar cells, horizontal cells, amacrine cells

d ganglion cells (Fig. 4). The photoreceptors, bipolar cells, and horizontal cells make

naptic contact in the outer retinal layer. The bipolar, amacrine, and ganglion cells make

ntact in the inner retinal layer (Husband & Shimizu, 2001).

e avian retina shows some interesting differences compared to mammals. It contains no

ood vessels; the pecten, a highly vascular structure, is responsible for providing nutrients and

ygen to the cells. Furthermore, it contains double cones, more richer intraretinal connections

e horizontal and amacrine cells (Hayes, 1982; Mariani, 1982, 1987), and complex ganglion

ll response properties (Pearlman & Hughes, 1976). Four different types of cones have been

served in the avian retina, whereas only three types of cones have been described in the

ammalian retina. The spectral sensitivity ranges from ultraviolet (320nm) to the far red

50nm) (Remy & Emmerton, 1991a). The presence of oil-droplets covering the cones add

other layer of complexity to the spectral composition of the photoreceptors in the retina.

Figure 4: Avian retina. The photoreceptors, bipolar cells, and horizontal cells make synaptic contact in the outer retinal layer. The bipolar, amacrine, and ganglion cells make contact in the inner retinal layer. Figure from Husband and Shimizu (2001).


24

The distribution of eye droplets in the retina defines two retinal areas (Fig. 5). The red field is

characterized by a high concentration of red and orange oil droplets and the yellow field with a

bigger concentration of yellow droplets.

P

RF

YFF

Figure 5: Schematic representation of the pigeons retina (modified from Galifret, 1968), where RF is the red field, YF is the yellow field, P is the pecten and F is the fovea centralis.

The red field located under the beak in the dorso-temporal retinal quadrant points into the

frontal visual field (Bloch & Martinoya, 1982b; Martin & Young, 1983; Martinoya, Rey, &

Bloch, 1981). Within the red field most birds also have an area of enhanced vision, the area

dorsalis which increases the acuity of the frontal binocular visual field (Martin & Katzir,

1999). This area is implicated in close sighting, feeding behaviour and the control of pecking

(Goodale, 1983).

The eyes of most birds are aligned laterally (Martin, 1993), which permits birds to receive and

process information of the lateral visual field through the yellow field. The lateral field also

contains an area of high ganglion cell density called the fovea centralis. This lateral visual

field serves far sighting, monitoring predators and conspecifics, as well as to detect food at

some distance (Fernndez-Juricic, Erichsen, & Kacelnik, 2004; Green et al., 1994). Hens tend

to view distant objects laterally while the preferentially observe objects less than 20-30 cm

away frontally (Dawkins, 2002).

Pigeons and some ground-foraging birds have a localized myopia in the temporal region. It can

be explained as an adaptation that permits pigeons to keep the ground in focus while foraging.

This localized myopia does not appear in the lateral visual field. In consequence, birds are

capable of maintaining in focus panoramic views and therefore monitor relevant information

like predators in the lateral visual field while foraging (Hodos & Erichsen, 1990).


25

The cyclopean area is the coverage of the total visual field of an animal around the head, that

is, the summation of the frontal and lateral visual fields (Martin & Katzir, 1999). Species with

large eyes have developed sunshade structures (e.g. eyebrows or eye lash-type feathering) and

larger blind areas to minimize sunlight glare (Martin & Katzir, 2000). Large blind areas

correspond to smaller cyclopean field, which might be reasonable in large species with low

predatory risk. However, species with small eyes generally have smaller blind areas and larger

cyclopean fields, because they may need a wider visual field for predators detection and are

not so strongly affected by sunlight (Fernndez-Juricic et al., 2004).

Martin and colleagues classified avian visual fields into 3 basic types and an additional

category (combination of two basic classes) (Martin et al., 2001; Martin & Coetzee, 2004;

Martin & Katzir, 1993, 1994, 1995, 1999, 2000).

Type 1. Visual guidance to food items taken in the bill: the visual projection of the bill tip

falls in the centre of the binocular region. The visual field is defined by an extensive cyclopean

field, with a long vertical but narrow binocular field. For example, rock pigeon, starling and

cattle egret.

Type 2. Non-visual guidance to food items taken with the bill: the projection of the bill falls

in the periphery of the visual field. A big cyclopean field is also expected with a narrow

binocular field, for example, Eurasian woodcock, mallard and teal.

Type 3. Non-visual guidance to food items taken with the feet: the projection of the bill fall

outside of the visual field. The blind area is relatively large and the binocular field is wide but

vertically small, for example tawny owl.

Combination of Types 1 and 3: similar to Type 1 in which individuals visually follow and take

mobile prey; but prey is taken with the feet, for example short-toed eagle.


26

1.5.2 Visual pathways in the avian brain

Two main visual pathways process visual information in birds: The thalamofugal pathway and

the tectofugal pathway (Fig. 6). The thalamofugal pathway corresponds to the geniculocortical

pathway in mammals, whereas the tectofugal pathway corresponds to the extrageniculocortical

pathway in mammals. These visual pathways are structurally and functionally independent,

although several connections and modulations between them have been described. The

accessory optic system in birds is a third independent visual pathway dedicated to optic flow,

self motion signals, and optokinetic stimulation processing.

Figure 6: Schematic overview of the thalamofugal (green) and tectofugal pathways (red). Abbreviations: E, entopallium; GLd, nucleus geniculatus lateralis, pars dorsalis; OT, optic tectum; Rt, nucleus rotundus.

P

RF

YFF

P

RF

YF

F

TO

E

left right

TO

Rt

E

left right

Gld

Wulst

CT+CP


27

1.5.2.1 Thalamofugal pathway

In pigeons, but not in chickens, the thalamofugal pathway receives visual input from the

yellow visual field (Gntrkn, Miceli, & Watanabe, 1993; Remy & Gntrkn, 1991), which

is transmitted to the contralateral thalamic nucleus geniculatus lateralis, pars dorsalis (GLd).

The GLd projects bilaterally to the visual wulst, a structure located in the telencephalon,

comparable to the striate cortex in mammals (Gntrkn, 2003; Jarvis et al., 2005).

In pigeons, the thalamofugal pathway mainly processes visual input from the lateral monocular

fields of the laterally placed eyes (Gntrkn & Hahmann, 1999; Remy & Gntrkn, 1991;

Vallortigara et al., 2001). However, in chicks, thalamofugal lesions affect frontal viewing in

chicks, suggesting that the thalamofugal system processes frontal visual field information in

chicks, but not in pigeons (Deng & Rogers, 2002).

In chicks, the thalamofugal system is asymmetrically structured by means of more contralateral

visual projections of the left nucleus geniculatus lateralis, pars dorsalis (GLd), to the right

hyperstriatum than vice versa (Deng & Rogers, 2002).

1.5.2.2 Tectofugal pathway

The tectofugal pathway processes visual information proceeding from the entire retina. The

visual input ascends from the retina to the contralateral optic tectum (OT), which projects

bilaterally to the entopallium (E) via the thalamic nucleus rotundus (Rt). The tectofugal

pathway is equivalent to the extrageniculocortical pathway in mammals: the optic tectum

corresponds to the superior colliculus, the nucleus rotundus to the lateral posterior-pulvinar,

and the entopallium to the extrastriate visual areas of the mammalian brain (Gntrkn, 2003;

Jarvis et al., 2005)

Morphological asymmetries have been found in the tectofugal system of the pigeon. In the

tectum and the Rt of pigeons, the soma size of visual cells is larger in the left hemisphere


28

(Gntrkn, 1997b; Manns & Gntrkn, 1999). The bilateral projections from the tectal

lamina 13 to the Rt lead to representations of both the ipsi- and the contralateral eye in the

tectofugal system of each hemisphere (Gntrkn, 2003). These ipsi- to contralareral

tectorotundal projections are asymmetric (Fig. 6). On the one hand, the quantity of ipsilateral

tectorotundal projections is similar. On the other hand, the number of neurons projecting

contralaterally from the right tectum to the left Rt are approximately twice in number than vice

versa. Therefore, the Rt on the left side receives a massive ipsilateral tectal input and also a

large number of afferents from the contralateral tectum (Gntrkn, Hellmann, Melsbach, &

Prior, 1998). Thus, the pigeons tectofugal system displays significant morphological

asymmetries which might be related to the behavioural lateralisation of the animals. In fact, the

left Rt is involved in acuity discrimination with the right and the left eye, whereas the right Rt

has minor relevance in participating in binocular acuity (Gntrkn & Hahmann, 1999).

Furthermore, there is evidence of asymmetries in the tectal and posterior commissures

connecting the tecta of both hemispheres. Field evoked potential (in response to a stroboscope

flash to the contralateral eye) recorded in the left and right tectum showed that the left-to-right

tectotectal modulation was more pronounced than vice versa (Keysers et al., 2000).

1.5.2.3 Tectofugal-thalamofugal projections

The tectofugal and thalamofugal pathways are not isolated systems, but they are interconnected

by projections from the thalamofugal system onto the tectofugal system and vice versa (Fig. 6

and Fig. 7). The visual wulst sends ipsilateral descending projections directly to the optic

tectum (Bagnoli et al., 1980; Karten, Hodos, Nauta, & Revzin, 1973; Miceli et al., 1987). This

projection is probably very important for the understanding of the functioning of the avian

visual system (Gntrkn et al., 1993). Recently, by recording from single units of the left and

right Rt of the tectofugal pathway, a modulation of the left visual wulst on both right and left

tectofugal systems has been described, whereas the right visual wulst showed only an

ipsilateral influence (Folta et al., 2004, Folta et al. in preparation).


29

P

RF

YFF

Tectum opticum

Lateral geniculate nucleus

Nucleus rotundus Entopallium

V. wulst

Figure 7: Schematic representation of the connections (in black) between the tectofugal (in red) and thalamofugal systems (in green).

Tectofugal-thalamofugal projections have been also described, radial neurons located in the

optic tectum project to the dorsolateral thalamus (Gamlin & Cohen, 1986; Wild, 1989).

Furthermore, the information processes by both ascending visual pathways converge into the

entopallium, thanks to projections from the visual wulst to the entopallium (Husband &

Shimizu, 1999; Karten & Hodos, 1970; Shimizu, Cox, & Karten, 1995; Watanabe, Ito, &

Ikushima, 1985). In zebra finches, the visual wulst has a significant facilitatory influence on

the processing of the contralateral visual information of the entopallium (Engelage & Bischof,

1994).

1.5.2.4 The accessory optic system

In addition to these two ascending visual pathways, the accessory optic system (AOS) is a

distinct visual pathway dedicated to the analysis of optic flow fields and various visual signals

generated by self-motion or optokinetic stimuli (Simpson, 1984). Given that head-bobbing is

triggered by optic flow (Friedman, 1975; Friedman, 1975b), it is widely accepted that the AOS

is involved in head-bobbing. Furthermore, AOS is considered to play a role in the stabilization

of the retinal image (Simpson, 1984; Westheimer & Blair, 1974), a function attributed to the

hold phase of head-bobbing.


30

Numerous electrophysiological studies have shown that neurons in the AOS exhibit direction

selectivity in response to large visual stimuli moving in the contralateral visual field (Frost,

Wylie, & Wang, 1990). Some neurons have binocular receptive fields that encode optic flow

fields induced by self-translation or self-rotation (Frost et al., 1990; Wylie & Frost, 1990;

Wylie, Glover, & Aitchison, 1999; Wylie, Glover, & Lau, 1998). In birds, the AOS consists of

the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (nLM).

The nBOR receives input from the retinal displaced ganglion cells, the visual forebrain, the

contralateral nBOR and the ipsilateral nucleus lentiformis mesencephali (nLM), and projects to

diverse regions including the contralateral nBOR, the ipsilateral nLM, the vestibulocerebellum

and the oculomotor complex (Frost & Wylie, 2000; Wang, Gu, & Wang, 2000).

Neurons of the nBOR directly project onto the Rt of the same hemisphere (Diekamp,

Hellmann, Troje, Wang, & Gntrkn, 2001). Furthermore, projections from the nBOR onto

the GLd have been described (Wylie, Bischof, & Frost, 1998; Wylie, Linkenhoker, & Lau,

1997). The data suggest that the AOS is able to modulate both thalamofugal and tectofugal

ascending visual pathways. It is plausible that these projections are necessary to distinguish

self- and object-motion processed by the AOS and the ascending pathways, respectively

(Diekamp et al., 2001).


The retina of the pigeon has two areas of enhanced vision: the red field in the dorsotemporal

retina pointing into the frontal binocular field and the yellow field projecting into the lateral

monocular field. The entire retina projects to the contralateral optic tectum and continues via

the diencephalic nucleus rotundus to the entopallium (tectofugal pathway). The monocular area

also projects to the contralateral geniculate thalamic nucleus and continues to the wulst

(thalamofugal pathway). These two different visual systems possibly operate independently in

the pigeons eye, however they are not isolated. Both pathways converge into the entopallium,

the visual wulst sends ipsilateral descending projections directly to the optic tectum, and finally

radial neurons located in the optic tectum project to the dorsolateral thalamus.


31

In addition to these two ascending visual pathways, the accessory optic system, consisting of

the nucleus of the basal optic root and the nucleus lentiformis mesencephali, is a distinct visual

pathway dedicated to the analysis of optic flow fields and various visual signals generated by

self-motion or optokinetic stimuli.

1.6 Goals of this work

The main aim of this work is to combine two aspects of the visual system in birds: on the one

hand to contribute to a better understanding of information transfer and its asymmetries, and on

the other hand to investigate the functional significance of head-bobbing in birds together with

its evolutionary basis.

The first part of this work investigates how information perceived in different parts of the

pigeons retinas, which is processes by two independent visual systems in each hemisphere, is

generalised in the pigeons brain. To achieve this aim, several experiments were designed. In

the first experiment and the third experiment, we tested intraocular transfer of information

between the red and the yellow fields in walking pigeons. In the second experiment, interocular

transfer of information between the yellow fields of both eyes was investigated.

It is believed that head-bobbing acts as an optokinetic behaviour allowing pattern recognition

during the hold phase. The aim of the fourth experiment was to clarify the role of the head-

bobbing hold and thrust phases in pattern recognition. Therefore, we conducted an

experimental task in which the pigeons needed to discriminate between two stimuli presented

either in the thrust phase, the hold phase, or randomly. To our knowledge, although head-

bobbing behaviour has been often discussed in the literature, few head-bobbing birds have

been listed until now. In the fifth experiment, a comprehensive list of head-bobbing and non

head-bobbing birds is offered. Furthermore, field observations, video recordings and

phylogenetic information, together with an analysis of behavioural and ecological characters,

were combined to clarify the adaptive value of head-bobbing and its evolutionary foundations.

General Methods 32

2. GENERAL METHODS

Many experiments reported until now

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Aves Trnasfer