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J Neurophysiol (April 1, 2003). 10.1152/jn.00832.2002
Submitted on Submitted 19 September 2002; accepted in final form 27 November
2002
Sobell Department of Neurophysiology, Institute of Neurology, Queen Square, London WC1N 3BG, United Kingdom
Baker, Stuart N.,
Elizabeth M. Pinches, and
Roger N. Lemon.
Synchronization in Monkey Motor Cortex During a Precision Grip
Task. II. Effect of Oscillatory Activity on Corticospinal Output. J. Neurophysiol. 89: 1941-1953, 2003. Recordings from primary motor cortex (M1) during periods of steady
contraction show oscillatory activity; these oscillations are coherent
with the activity of contralateral muscles. We investigated synchronization of corticospinal output neurons with the oscillations, which could provide the pathway for their transmission to the spinal
motoneurons. One hundred seventy-six antidromically identified pyramidal tract neurons (PTNs) were recorded from M1 in three macaque
monkeys trained to perform a precision grip task. Local field
potentials (LFP) were simultaneously recorded. All analysis was
confined to the hold period of the task, where our previous work has
shown that there is the strongest oscillatory activity. Coherence was
calculated between LFP and PTN discharge. Significant coherence was
seen in three bands, with frequencies of 10-14, 17-31, and 34-44 Hz.
Coherence values were low, with the majority of PTN-LFP coherences
having a peak lower than 0.05. The phase of coherence was approximately
/2 radians for each band (with LFP polarity defined as negative
upward), although there was some dispersion of phase across the
population of PTNs. Coherence was also calculated between pairs of PTNs
that had been simultaneously recorded. Where there was significant
coherence, it was also generally smaller than 0.05. The phase of
PTN-PTN coherence clustered around zero radians. A computer model was
constructed to assist the interpretation of the experimental results.
It simulated an integrate-and-fire neuron responding to synaptic
inputs. A fraction of the synaptic inputs was synchronized with a
simulated LFP; the remainder were uncorrelated with it. The model
showed that coherence between the LFP and the output spike train
considerably underestimated the fraction of synchronized inputs.
Additionally, for a given fraction of synchronized inputs, coherence
was smaller for high- compared with low-frequency bins. Cell discharge
rate also influenced the spike-LFP coherence: coherence was higher for
simulations in which the cell discharged at a faster rate. Thus
although levels of PTN-LFP coherence seen experimentally were low, a
considerable proportion of the input to the PTN must be synchronized
with the global oscillatory activity recorded by the LFP. The low
LFP-PTN coherences do however indicate that cortical oscillations are transmitted with only low fidelity in the discharge of a single PTN.
Using further computer simulations, it was demonstrated that a small
population of PTNs could encode the cortical oscillatory signal
effectively, since the action of averaging across the population improves the signal:noise ratio. The oscillations will therefore be
effectively transmitted to spinal motoneurons, and this has important
consequences for the possible role of oscillations in motor control of
the hand.
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