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The Journal of Neurophysiology Vol. 81 No. 3 March 1999, pp. 1057-1074
Copyright ©1999 by the American Physiological Society
Institut National de la Santé et de la Recherche Médicale U. 371, Cerveau et Vision, 69675 Bron Cedex, France
Nowak, L. G.,
M.H.J. Munk,
A. C. James,
P. Girard, and
J. Bullier.
Cross-correlation study of the temporal interactions between areas V1
and V2 of the macaque monkey. Cross-correlation studies performed in cat visual cortex have shown that neurons in different cortical areas of the same hemisphere or in corresponding areas of
opposite hemispheres tend to synchronize their activities. The presence
of synchronization may be related to the parallel organization of the
cat visual system, in which different cortical areas can be activated
in parallel from the lateral geniculate nucleus. We wanted to determine
whether interareal synchronization of firing can also be observed in
the monkey, in which cortical areas are thought to be organized in a
hierarchy spanning different levels. Cross-correlation histograms
(CCHs) were calculated from pairs of single or pairs of multiunit
activities simultaneously recorded in areas V1 and V2 of paralyzed and
anesthetized macaque monkeys. Moving bars and flashed bars were used as
stimuli. The shift predictor was calculated and subtracted from the raw
CCH to reveal interactions of neuronal origin in isolation. Significant CCH peaks, indicating interactions of neuronal origin, were obtained in
11% of the dual single-unit recordings and 46% of the dual multiunit
recordings with moving bars. The incidence of nonflat CCHs with flashed
bars was 29 and 78%, respectively. For the pairs of recording sites
where both flashed and moving stimuli were used, the incidences of
significant CCHs were very similar. Three types of peaks were
distinguished on the basis of their width at half-height: T (<16 ms),
C (between 16 and 180 ms), and H peaks (>180 ms). T peaks were very
rarely observed (<1% in single-unit recordings). H peaks were
observed in 7-16% of the single-unit CCHs, and C peaks in 6-16%,
depending on the stimulus used. C and H peaks were observed more often
when the receptive fields were overlapping or distant by <2°. To
test for the presence of synchronization between neurons in areas V1
and V2, we measured the position of the CCH peak with respect to the
origin of the time axis of the CCH. Only in the case of a few T peaks
did we find displaced peaks, indicating a possible drive of the V2
neuron by the simultaneously recorded V1 cell. All the other peaks were either centered on the origin or overlapped the origin of time with
their upper halves. Thus similarly to what has been reported for the
cat, neurons belonging to different cortical areas in the monkey tend
to synchronize the time of emission of their action potentials with
three different levels of temporal precision. For peaks calculated from
flashed stimuli, we compared the peak position with the difference
between latencies of V1 and V2 neurons. There was a clear correlation
for single-unit pairs in the case of C peaks. Thus the position of a C
peak on the time axis appears to reflect the order of visual activation
of the correlated neurons. The coupling strength for H peaks was
smaller during visual drive compared with spontaneous activity. On the
contrary, C peaks were seen more often and were stronger during visual
stimulation than during spontaneous activity. This suggests that C-type
synchronization is associated with the processing of visual
information. The origin of synchronized activity in a serially
organized system is discussed.
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