Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex
- Timo van Kerkoerlea,1,
- Matthew W. Selfa,
- Bruno Dagninoa,
- Marie-Alice Gariel-Mathisa,
- Jasper Poorta,
- Chris van der Togta, and
- Pieter R. Roelfsemaa,b,c,1
- aDepartment of Vision and Cognition, Netherlands Institute for Neurosciences, Royal Netherlands Academy of Arts and Sciences (KNAW), 1105 BA, Amsterdam, The Netherlands;
- bDepartment of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Vrije Universiteit, 1081HV, Amsterdam, The Netherlands; and
- cPsychiatry Department, Academic Medical Center, 1105 AZ, Amsterdam, The Netherlands
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Edited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved August 8, 2014 (received for review February 22, 2014)
Significance
One of the main unresolved questions in cognitive neuroscience is how low-level and high-level areas of the visual cortex interact with each other during perception and cognition. We investigated whether cortical oscillations can be used to distinguish feedforward from feedback processing. We studied the propagation of α- and γ-oscillations through the cortical layers and between different visual cortical areas. We induced oscillations in different areas with microstimulation and influenced them using a pharmacological approach. The results of these experiments demonstrate that γ-oscillations propagate in the feedforward direction, whereas α-oscillations propagate in the feedback direction. We conclude that high- and low-frequency oscillations provide markers of feedforward and feedback processing, respectively.
Abstract
Cognitive functions rely on the coordinated activity of neurons in many brain regions, but the interactions between cortical areas are not yet well understood. Here we investigated whether low-frequency (α) and high-frequency (γ) oscillations characterize different directions of information flow in monkey visual cortex. We recorded from all layers of the primary visual cortex (V1) and found that γ-waves are initiated in input layer 4 and propagate to the deep and superficial layers of cortex, whereas α-waves propagate in the opposite direction. Simultaneous recordings from V1 and downstream area V4 confirmed that γ- and α-waves propagate in the feedforward and feedback direction, respectively. Microstimulation in V1 elicited γ-oscillations in V4, whereas microstimulation in V4 elicited α-oscillations in V1, thus providing causal evidence for the opposite propagation of these rhythms. Furthermore, blocking NMDA receptors, thought to be involved in feedback processing, suppressed α while boosting γ. These results provide new insights into the relation between brain rhythms and cognition.
Footnotes
- ↵1To whom correspondence may be addressed. Email: p.roelfsema{at}nin.knaw.nl or t.van.kerkoerle{at}nin.knaw.nl.
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This Feature Article is part of a series identified by the Editorial Board as reporting findings of exceptional significance.
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Author contributions: T.v.K. and P.R.R. designed research; T.v.K., M.W.S., B.D., M.-A.G.-M., and J.P. performed research; T.v.K. and C.v.d.T. contributed new analytic tools; T.v.K. analyzed data; and T.v.K. and P.R.R. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
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See Commentary on page 14316.
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This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1402773111/-/DCSupplemental.
Freely available online through the PNAS open access option.
