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The Journal of Neurophysiology Vol. 86 No. 4 October 2001, pp. 1700-1716
Copyright ©2001 by the American Physiological Society
1School of Psychology, University of St. Andrews, Fife KY16 9JU, United Kingdom; 2Department of Neuroscience, Brown University, Providence, Rhode Island 02912; and 3National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
Oram, Mike W.,
Nicholas
G. Hatsopoulos,
Barry J. Richmond, and
John P. Donoghue.
Excess Synchrony in Motor Cortical Neurons Provides Redundant
Direction Information With That From Coarse Temporal Measures. J. Neurophysiol. 86: 1700-1716, 2001. Previous studies have shown that measures of fine temporal
correlation, such as synchronous spikes, across responses of motor cortical neurons carries more directional information than that predicted from statistically independent neurons. It is also known, however, that the coarse temporal measures of responses, such as spike
count, are not independent. We therefore examined whether the
information carried by coincident firing was related to that of
coarsely defined spike counts and their correlation. Synchronous spikes
were counted in the responses from 94 pairs of simultaneously recorded
neurons in primary motor cortex (MI) while monkeys performed arm
movement tasks. Direct measurement of the movement-related information
indicated that the coincident spikes (1- to 5-ms precision) carry
~10% of the information carried by a code of the two spike counts.
Inclusion of the numbers of synchronous spikes did not add information
to that available from the spike counts and their coarse temporal
correlation. To assess the significance of the numbers of coincident
spikes, we extended the stochastic spike count matched (SCM) model to
include correlations between spike counts of the individual neural
responses and slow temporal dependencies within neural responses (~30
Hz bandwidth). The extended SCM model underestimated the numbers of
synchronous spikes. Therefore as with previous studies, we found that
there were more synchronous spikes in the neural data than could be
accounted for by this stochastic model. However, the SCM model accounts
for most (R2 = 0.93 ± 0.05, mean ± SE) of the differences in the observed number of
synchronous spikes to different directions of arm movement, indicating
that synchronous spiking is directly related to spike counts and their
broad correlation. Further, this model supports the information
theoretic analysis that the synchronous spikes do not provide
directional information beyond that available from the firing rates of
the same pool of directionally tuned MI neurons. These results show
that detection of precisely timed spike patterns above chance levels
does not imply that those spike patterns carry information unavailable
from coarser population codes but leaves open the possibility that
excess synchrony carries other forms of information or serves other
roles in cortical information processing not studied here.
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