Theta, but Not Gamma Oscillations in Area V4 Depend on Input from Primary Visual Cortex

Ricardo Kienitz,Michele A Cox,Kacie Dougherty,Richard C Saunders,Joscha T Schmiedt,David A Leopold,Alexander Maier,Michael C Schmid

doi:10.1016/j.cub.2020.10.091

Abstract

Theta (3-9Hz) and gamma (30-100Hz) oscillations have been observed at different levels along the hierarchy of cortical areas and across a wide set of cognitive tasks. In the visual system, the emergence of both rhythms in primary visual cortex (V1) and mid-level cortical areas V4 has been linked with variations in perceptual reaction times.1-5 Based on analytical methods to infer causality in neural activation patterns, it was concluded that gamma and theta oscillations might both reflect feedforward sensory processing from V1 to V4.6-10 Here, we report on experiments in macaque monkeys in which we experimentally assessed the presence of both oscillations in the neural activity recorded from multi-electrode arrays in V1 and V4 before and after a permanent V1 lesion. With intact cortex, theta and gamma oscillations could be reliably elicited in V1 and V4 when monkeys viewed a visual contour illusion and showed phase-to-amplitude coupling. Laminar analysis in V1 revealed that both theta and gamma oscillations occurred primarily in the supragranular layers, the cortical output compartment of V1. However, there was a clear dissociation between the two rhythms in V4 that became apparent when the major feedforward input to V4 was removed by lesioning V1: although V1 lesioning eliminated V4 theta, it had little effect on V4 gamma power except for delaying its emergence by >100ms. These findings suggest that theta is more tightly associated with feedforward processing than gamma and pose limits on the proposed role of gamma as a feedforward mechanism.

Highlights

MethodsMETHOD DETAILSParts of the dataset underlying this study (V4 data from monkey B and F) have been analyzed and published with regard to the dependence of a Kanizsa-specific increase in single (and multi-) unit spiking on the receptive field focus[57]
Analysis of V1 local field potential (LFP) revealed that all channels showed theta and gamma power increases following visual stimulation
The emergence of both rhythms in primary visual cortex (V1) and mid-level cortical areas V4 has been linked with variations in perceptual reaction times.[1,2,3,4,5]

Summary

Methods

METHOD DETAILSParts of the dataset underlying this study (V4 data from monkey B and F) have been analyzed and published with regard to the dependence of a Kanizsa-specific increase in single (and multi-) unit spiking on the receptive field focus[57]. The Kanizsa illusion and the control stimulus consisted of four inducers ($1 diameter) located at (1, À1), (3, À1), (1, À3) and (3, À3), presented for 1 s (1.5 s in V1 recordings) after 1 s of fixation baseline. Each inducer consisted of a white disk with one quarter of the circle colored in red, giving them a ‘‘pacman-like’’ appearance. The control stimulus consisted of inducers that were rotated by 180 such that the red cutouts were facing outward (CF1 in[57]). For monkey K, the stimulus position was adapted to the V1 receptive fields (center of stimulus: x = 1, y = À4.2). For the laminar V1 recordings, the Kanizsa stimulus and its control were positioned such that the receptive field focus (RFF, see57) of the recording site was centered on the illusory parts of the stimulus

Results

Discussion

Conclusion