Three distinct gamma oscillatory networks within cortical columns in macaque monkeys' area V1.

Abstract

Introduction: A fundamental property of the neocortex is its columnar organization in many species. Generally, neurons of the same column share stimulus preferences and have strong anatomical connections across layers. These features suggest that neurons within a column operate as one unified network. Other features, like the different patterns of input and output connections of neurons located in separate layers and systematic differences in feature tuning, hint at a more segregated and possibly flexible functional organization of neurons within a column.

Methods: To distinguish between these views of columnar processing, we conducted laminar recordings in macaques' area V1 while they performed a demanding attention task. We identified three separate regions with strong gamma oscillatory activity, located in the supragranular, granular, and infragranular laminar domains, based on the current source density (CSD).

Results and discussion: Their characteristics differed significantly in their dominant gamma frequency and attention-dependent modulation of their gramma power and gamma frequency. In line, spiking activity in the supragranular, infragranular, and upper part of the granular domain exhibited strong phase coherence with the CSD signals of their domain but showed much weaker coherence with the CSD signals of other domains.

Conclusion: These results indicate that columnar processing involves a certain degree of independence between neurons in the three laminar domains, consistent with the assumption of multiple, separate intracolumnar ensembles. Such a functional organization offers various possibilities for dynamic network configuration, indicating that neurons in a column are not restricted to operate as one unified network. Thus, the findings open interesting new possibilities for future concepts and investigations on flexible, dynamic cortical ensemble formation and selective information processing.