The role of neuronal synchronization in response selection: a biologically plausible theory of structured representations in the visual cortex.

Abstract Recent experimental results in the visual cortex of cats and monkeys have suggested an important role for synchronization of neuronal activity on a millisecond time scale. Synchronization has been found to occur selectively between neuronal responses to related image components. This suggests that not only the firing rates of neurons but also the relative timing of their action potentials is used as a coding dimension. Thus, a powerful relational code would be available, in addition to the rate code, for the representation of perceptual objects. This could alleviate difficulties in the simultaneous representation of multiple objects. In this article we present a set of theoretical arguments and predictions concerning the mechanisms that could group neurons responding to related image components into coherently active aggregates. Synchrony is likely to be mediated by synchronizing connections; we introduce the concept of an interaction skeleton to refer to the subset of synchronizing connections that are rendered effective by a particular stimulus configuration. If the image is segmented into objects, these objects can typically be segmented further into their constituent parts. The synchronization behavior of neurons that represent the various image components may accurately reflect this hierarchical clustering. We propose that the range of synchronizing interactions is a dynamic parameter of the cortical network, so that the grain of the resultant grouping process may be adapted to the actual behavioral requirements. It can be argued that different aspects of purposeful behavior rely on separable processes by which sensory input is transformed into adjustments of motor activity. Indeed, neurophysiological evidence has suggested separate processing streams originating in the primary visual cortex for object identification and sensorimotor coordination. However, such a separation calls for a mechanism that avoids interference effects in the presence of multiple objects, or when multiple motor programs are simultaneously prepared. In this article we suggest that synchronization between responses of neurons in both the visual cortex and in areas that are involved in response selection and execution might allow for a selective routing of sensory information to the appropriate motor program.