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Evidence that Synchronized Motor Unit Firings Are Epiphenomena of the Onion Skin Property Not Common Inputs Joshua C. Kline a,b and Carlo J. De Luca a,b a) Delsys Inc., Natick, MA, USA; b) Department of Biomedical Engineering, Boston University, Boston, MA, USA Synchronous motor unit (MU) firing instances have been attributed to anatomical inputs shared by motoneurons. Yet, there is a lack of empirical evidence confirming the notion that common inputs are responsible fro synchronization during voluntary conditions. Therefore, we designed two experiments to: 1) test the veracity of the common input notion; and 2) investigate alternative empirically-based explanations for synchronization. References De Luca et al, J Neurophysiol (1993) De Luca and Contessa, J Neurophysiol (2012) De Luca and Kline, J Neurophysiol (2014) Motivation Experiment 1: Testing the Common Input Notion Subjects were required to track a two-force level paradigm that was maintained at a relatively low force level and then increased to a relatively higher force level. We used the dEMG System for decomposing sEMG signals into MU action potential trains (MUAPTs) and compared the degree of synchronization measured by the SigMax method (De Luca and Kline, 2014) between MUAPTs as their firing rates progressed throughout the increasing force contraction. This work was supported in part by two grants from NIH 1R43NS077526, and a grant from the Neuromuscular Research Foundation. Acknowledgements Experiment 1: Testing The Common Input Notion The common input notion provides no empirically supported explanation to account for the decrease in synchronization with increasing contraction force. Thus, the practice of inferring anatomical connections shared by motoneurons based on observations of synchronization remains empirically unsupported. So viewed, occasionally synchronous firing instances are likely an epiphenomenon, subject to countless unknown neural interactions. As such, synchronization may not be the product of a specific design and may not serve a specific physiological purpose. Our explanation for synchronization has the advantage of being supported by empirical evidence; whereas, the common input does not. Experiment Experiment 2: Investigating Empirical Relationships with Synchronization We studied associations between synchronization and MU firing rates in different muscles and for different voluntary contraction force levels by measuring the synchronization index (SI) between pairs of MUAPTs active during voluntary contractions ranging from 5% MVC to 50% MVC in the first dorsal interosseous (FDI) and vastus lateralis (VL) muscles. Measure Synchronization Measure Synchronization Lower Force Level Higher Force Level Compare MU A MU B MU Mean Firing Rate MU Mean Firing Rate Low High Low High Synchronization Measurements 2 3 1 High Sync. Low Sync. No Sync. 1) SI = 30.2 2) SI = 17.5 3) SI = 0 MU Mean Firing Rates 2 3 1 . . . 5 10 15 20 0 10 20 30 40 Time (s) Mean Firing Rate (pps) 0 0 5 10 15 20 25 Force (% MVC) -25 0 25 0 1 -10 0 10 0 1 Latency(ms) Latency(ms) Probability Probability -10 10 0 We measured synchronization between the same pairs of MUAPTs as their firing rates progressed from a contraction at a relatively low force level to a higher one. As the contraction force increased, synchronization decreased. FDI VL Sync. Index (%) -15 0 15 10 5 -5 -10 Alt. MUAPT MFR (pps) 10 20 Alt. MUAPT MFR (pps) 10 20 10 20 Ref. MUAPT MFR (pps) Sync. Index (%) -15 0 15 10 5 -5 -10 Avg. MUAPT MFR (pps) 10 20 Avg. MUAPT MFR (pps) 10 20 G) SI H) SI Sync. Index (%) -15 0 15 10 5 -5 -10 E) SI < 0 (p<0.0001) F) SI < 0 (p<0.0001) Low Force High Force SI SI Our data set of 17,546 paired MUAPTs revealed that the degree of synchronization varies as a function of two characteristics of the firing rate: the slope and similarity of the firing rates. Both are measures of the excitation of the motoneurons (De Luca and Contessa, 2012). As the force generated by the muscle increases the firing rate slope decreases and the synchronization correspondingly decreases. Different muscles have motor units with different firing rate characteristics, and display different amounts of synchronization. 1 1 3 2 More Sync. Similar firing rates Steep slopes Moderate Sync. Less Sync. No Sync. Different firing rates Similar firing rates Moderate slopes Lower Voluntary Excitation Higher Voluntary Excitation Similar firing rates Shallow slopes Firing Rate Force Firing Rate Force Firing Rate Force 0 10 20 30 40 50 60 70 0 5 10 15 20 25 30 Time (s) Mean Firing Rate (pps) 0 5 10 15 20 Force (% MVC) MU 2 MU 3 MU 14 MU 17 Experiment 2: New Explanation for Synchronization A) SI at Lower Force B) SI at Lower Force D) SI at Higher Force C) SI at Higher Force Sync. Index (%) 0 10 20 30 Ref. MUAPT MFR (pps) 10 20 Ref. MUAPT MFR (pps) 10 20 Sync. Index (%) 0 10 20 30 Avg. MUAPT MFR (pps) 10 20 Avg. MUAPT MFR (pps) 10 20 3 1 1 2 Synchronization Decreases with Increasing Force “Common Input” Provides no Explanation Synchronization is Related to the Characteristics of the Motor Unit Firing Rates SENSORS FOR MOVEMENT SCIENCES

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Page 1: Evidence that Synchronized Motor Unit Firings Are

Evidence that Synchronized Motor Unit Firings Are

Epiphenomena of the Onion Skin Property Not Common Inputs

Joshua C. Klinea,b and Carlo J. De Lucaa,b

a) Delsys Inc., Natick, MA, USA; b) Department of Biomedical Engineering, Boston University, Boston, MA, USA

Synchronous motor unit (MU) firing instances have been attributed to anatomical

inputs shared by motoneurons. Yet, there is a lack of empirical evidence confirming the

notion that common inputs are responsible fro synchronization during voluntary

conditions. Therefore, we designed two experiments to:

1) test the veracity of the common input notion; and

2) investigate alternative empirically-based explanations for synchronization.

References

De Luca et al, J Neurophysiol (1993)

De Luca and Contessa, J Neurophysiol (2012)

De Luca and Kline, J Neurophysiol (2014)

Motivation

Experiment 1: Testing the Common Input Notion

Subjects were required to track a two-force level paradigm that was maintained at a

relatively low force level and then increased to a relatively higher force level. We used

the dEMG System for decomposing sEMG signals into MU action potential trains

(MUAPTs) and compared the degree of synchronization measured by the SigMax

method (De Luca and Kline, 2014) between MUAPTs as their firing rates progressed

throughout the increasing force contraction.

This work was supported in part by two

grants from NIH 1R43NS077526, and a grant

from the Neuromuscular Research

Foundation.

Acknowledgements

Experiment 1: Testing The Common Input Notion

The common input notion provides no empirically supported explanation to account

for the decrease in synchronization with increasing contraction force.

Thus, the practice of inferring anatomical connections shared by motoneurons based

on observations of synchronization remains empirically unsupported.

So viewed, occasionally synchronous firing instances are likely an epiphenomenon,

subject to countless unknown neural interactions. As such, synchronization may not be

the product of a specific design and may not serve a specific physiological purpose.

Our explanation for synchronization has the advantage of being supported by

empirical evidence; whereas, the common input does not.

Experiment

Experiment 2: Investigating Empirical Relationships with Synchronization

We studied associations between synchronization and MU firing rates in different

muscles and for different voluntary contraction force levels by measuring the

synchronization index (SI) between pairs of MUAPTs active during voluntary

contractions ranging from 5% MVC to 50% MVC in the first dorsal interosseous (FDI)

and vastus lateralis (VL) muscles.

Measure Synchronization

Measure Synchronization

Lower Force Level

Higher Force Level

Compare

……

MU A

MU B

MU Mean Firing Rate

MU

Mea

n F

iring

Rat

e

Low High

Low

Hig

h

Synchronization Measurements

2

31

High Sync.

Low Sync.

No Sync.

1) SI = 30.2

2) SI = 17.5

3) SI = 0

MU Mean Firing Rates

2

31

..

.

5 10 15 200

10

20

30

40

Time (s)

Mea

n F

iring

Rat

e (p

ps)

00

5

10

15

20

25

For

ce (

% M

VC

)

-25 0 250

1

-10 0 10

0

1

Latency(ms) Latency(ms)

Pro

babi

lity

Pro

babi

lity

-10 100

We measured synchronization between the same pairs of MUAPTs as their firing rates

progressed from a contraction at a relatively low force level to a higher one. As the

contraction force increased, synchronization decreased.

FDI VL

∆ S

ync.

Inde

x (%

)

-15

0

15

10

5

-5

-10

Alt. MUAPT MFR (pps)

10 20

Alt. MUAPT MFR (pps)

10 20

10

20

Ref

. MU

AP

T M

FR

(pp

s)

∆ S

ync.

Inde

x (%

)

-15

0

15

10

5

-5

-10

Avg. MUAPT MFR (pps)

10 20

Avg. MUAPT MFR (pps)

10 20

G) ∆SI H) ∆SI

∆ S

ync.

Inde

x (%

)

-15

0

15

10

5

-5

-10

E) ∆SI < 0 (p<0.0001) F) ∆SI < 0 (p<0.0001)

Low Force

HighForce

∆SI

∆SI

Our data set of 17,546 paired MUAPTs revealed that the degree of synchronization

varies as a function of two characteristics of the firing rate: the slope and similarity of

the firing rates. Both are measures of the excitation of the motoneurons (De Luca and

Contessa, 2012). As the force generated by the muscle increases the firing rate slope

decreases and the synchronization correspondingly decreases. Different muscles have

motor units with different firing rate characteristics, and display different amounts of

synchronization.

1 1

3

2

MoreSync.

Similar firing ratesSteep slopes

ModerateSync.

LessSync.

No Sync.

Different firing rates

Similar firing ratesModerate slopes

Lower Voluntary Excitation

Higher Voluntary Excitation

Similar firing ratesShallow slopes

Firi

ng R

ate

Force

Firi

ng R

ate

Force

Firi

ng R

ate

Force

0 10 20 30 40 50 60 70

0

5

10

15

20

25

30

Time (s)

Mea

n F

iring

Rat

e (p

ps)

0

5

10

15

20

For

ce (

% M

VC

)

MU 2

MU 3

MU 14

MU 17

Experiment 2: New Explanation for Synchronization

A) SI at Lower Force B) SI at Lower Force

D) SI at Higher ForceC) SI at Higher Force

Syn

c. In

dex

(%)

0

10

20

30

Ref

. MU

AP

T M

FR

(pp

s)

10

20

Ref

. MU

AP

T M

FR

(pp

s)

10

20

Syn

c. In

dex

(%)

0

10

20

30

Avg. MUAPT MFR (pps)

10 20

Avg. MUAPT MFR (pps)

10 20

31 1

2

Synchronization Decreases with Increasing Force

“Common Input” Provides no Explanation

Synchronization is Related to the Characteristics of the

Motor Unit Firing Rates

SENSORS FOR MOVEMENT SCIENCES