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The Journal of Neurophysiology Vol. 84 No. 4 October 2000, pp. 1770-1780
Copyright ©2000 by the American Physiological Society
Sobell Department of Neurophysiology, Institute of Neurology, London WC1N 3BG, United Kingdom
Baker, Stuart N. and
Roger N. Lemon.
Precise Spatiotemporal Repeating Patterns in Monkey Primary and
Supplementary Motor Areas Occur at Chance Levels. J. Neurophysiol. 84: 1770-1780, 2000. Precise
spatiotemporal patterns in neural discharge are a possible mechanism
for information encoding in the brain. Previous studies have found that
such patterns repeat and appear to relate to key behavioral events.
Whether these patterns occur above chance levels remains controversial.
To address this question, we have made simultaneous recordings from
between two and nine neurons in the primary motor cortex and
supplementary motor area of three monkeys while they performed a
precision grip task. Out of a total of 67 neurons, 46 were
antidromically identified as pyramidal tract neurons. Sections of
recordings 60 s long were searched for patterns involving three or
more spikes that repeated at least twice. The allowed jitter for
pattern repetition was 3 ms, and the pattern length was limited to 192 ms. In all 11 recordings analyzed, large numbers of repeating patterns
were found. To assess the expected chance level of patterns,
"surrogate" datasets were generated. These had the same
moment-by-moment modulation in firing rate as the experimental spike
trains, and matched their interspike interval distribution, but did not
preserve the precise timing of individual spikes. The number of
repeating patterns in 10 randomly generated surrogates was used to form
99% confidence limits on the repeating pattern count expected by
chance. There was close agreement between these confidence limits and
the number of patterns seen in the experimental data. Analysis of high
complexity patterns was carried out in four long recordings (mean
duration 23.2 min, mean number of neurons simultaneously recorded 7.5).
This analysis logged only patterns composed of a larger number (7-11)
of spikes. The number of patterns seen in the surrogate datasets showed
a small but significant excess over those seen in the original
experimental data; this is discussed in the context of surrogate
generation. The occurrence of repeating patterns in the experimental
data were strongly associated with particular phases of the precision grip task; however, a similar task dependence was seen for the surrogate data. When a repeating pattern was used as a template to find
inexact matches, in which up to half of the component spikes could be
missing, similar numbers of matches were found in experimental and
surrogate data, and the time of occurrence of such matches showed the
same task dependence. We conclude that the existence of precise
repeating patterns in our data are not due to cortical mechanisms that
favor this form of coding, since as many, if not more, patterns are
produced by spike trains constructed only to modulate their firing rate
in the same way as the experimental data, and to match the interspike
interval histograms. The task dependence of pattern occurrence is
explicable as an artifact of the modulation of neural firing rate. The
consequences for theories of temporal coding in the cortex are discussed.
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