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

Lookup NU author(s): Dr Ricardo Kienitz, Professor Michael SchmidORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2020 The Author(s). Theta (3–9 Hz) and gamma (30–100 Hz) 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 >100 ms. 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.© 2020 The Author(s)Kienitz et al. show that, upon visual stimulation, V1 and V4 show theta and gamma oscillations, which interacted in terms of phase-to-amplitude coupling. Lesion of V1, the major input source to V4, eliminated V4 theta oscillations. In contrast, V4 gamma oscillations were less affected and still contained stimulus information but emerged delayed (>100 ms).


Publication metadata

Author(s): Kienitz R, Cox MA, Dougherty K, Saunders RC, Schmiedt JT, Leopold DA, Maier A, Schmid MC

Publication type: Article

Publication status: Published

Journal: Current Biology

Year: 2021

Volume: 31

Issue: 3

Pages: 635-642.e3

Print publication date: 08/02/2021

Online publication date: 04/12/2020

Acceptance date: 29/10/2020

Date deposited: 04/06/2021

ISSN (print): 0960-9822

ISSN (electronic): 1879-0445

Publisher: Cell Press

URL: https://doi.org/10.1016/j.cub.2020.10.091

DOI: 10.1016/j.cub.2020.10.091


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Funding

Funder referenceFunder name
1R01EY027402-02
2806/1
2T32 EY007135-21
637638Commission of the European Communities
ZIAMH002838

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