Journal of Neuroscience, Vol 16, 2381-2396, Copyright © 1996 by Society for Neuroscience
Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey
AK Kreiter and W Singer
Max Planck Institute for Brain Research, Frankfurt/Main, Germany.
In visual areas of the cerebral cortex, most neurons exhibit preferences
for particular features of visual stimuli, but in general, the tuning is
broad. Thus, even simple stimuli evoke responses in numerous neurons with
differing but overlapping feature preferences, and it is commonly held that
a particular feature is encoded in the pattern of graded responses of the
activated population rather than in the optimal responses of individual
cells. To decipher this population code, responses evoked by a particular
stimulus need to be identified and bound together for further joint
processing and must not be confounded with responses to other, nearby
stimuli. Such selection of related responses could be achieved by
synchronizing the respective discharges at a time scale of milliseconds, as
this would selectively and jointly enhance their saliency. This hypothesis
predicts that a given set of neurons should exhibit synchronized discharges
more often when responding to a single stimulus than when activated by
different but simultaneously presented stimuli. To test this prediction,
recordings were performed with two electrodes from spatially segregated
cells in the middle temporal area (MT) of the awake behaving macaque
monkey. It was found that cells with overlapping receptive fields, but
different preferences for directions of motion, can engage in synchronous
activity if they are stimulated with a single moving bar. In contrast, if
the same cells are activated with two different bars, each moving in the
direction preferred by the cells at the two respective sites, responses
show no or much fewer synchronous epochs. Control experiments exclude that
this effect is attributable to changes in response amplitude, the mere
presence of two stimuli, or the specific orientation of the bars. The
critical variable determining the strength of correlation is the extent to
which both sites are activated by a common stimulus or by two different
stimuli with different directions of motion.