Routing information flow by separate neural synchrony frequencies allows for “functionally labeled lines” in higher primate cortex

Significance Dynamical coordination of the neural activity between individual neurons is known to have a key role in the efficient transfer of sensory information to associative areas. Here, we report a role of interneuronal synchrony within the high-gamma (180 to 220 Hz) frequency range of activity in macaque area MT (a visual area in the dorsal visual pathway) in determining behavioral performance. This is, however, in contrast to previous reports for the ventral visual pathway (such as area V4), where only gamma range (40 to 70 Hz) was observed to play a role. We propose that such a difference between the functional coordination in different visual pathways might be used to unambiguously identify the source of input to the higher areas. Efficient transfer of sensory information to higher (motor or associative) areas in primate visual cortical areas is crucial for transforming sensory input into behavioral actions. Dynamically increasing the level of coordination between single neurons has been suggested as an important contributor to this efficiency. We propose that differences between the functional coordination in different visual pathways might be used to unambiguously identify the source of input to the higher areas, ensuring a proper routing of the information flow. Here we determined the level of coordination between neurons in area MT in macaque visual cortex in a visual attention task via the strength of synchronization between the neurons’ spike timing relative to the phase of oscillatory activities in local field potentials. In contrast to reports on the ventral visual pathway, we observed the synchrony of spikes only in the range of high gamma (180 to 220 Hz), rather than gamma (40 to 70 Hz) (as reported previously) to predict the animal’s reaction speed. This supports a mechanistic role of the phase of high-gamma oscillatory activity in dynamically modulating the efficiency of neuronal information transfer. In addition, for inputs to higher cortical areas converging from the dorsal and ventral pathway, the distinct frequency bands of these inputs can be leveraged to preserve the identity of the input source. In this way source-specific oscillatory activity in primate cortex can serve to establish and maintain “functionally labeled lines” for dynamically adjusting cortical information transfer and multiplexing converging sensory signals.