Theta-gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

Authors

Benjamin Voloh, Department of Biology, Centre for Vision Research, York University, Toronto, ON M6J 1P3, Canada;
Taufik A. Valiante, Division of Fundamental Neurobiology, Toronto Western Research Institute, Toronto, ON M5T 2S8, Canada; Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, ON M5T 1P5, Canada;
Stefan Everling, Department of Physiology and Pharmacology, Centre for Functional and Metabolic Mapping, University of Western Ontario, London, ON N6A 5B7, Canada.
Thilo Womelsdorf, Department of Biology, Centre for Vision Research, York University, Toronto, ON M6J 1P3, Canada; Department of Physiology and Pharmacology, Centre for Functional and Metabolic Mapping, University of Western Ontario, London, ON N6A 5B7, Canada thiwom@yorku.ca.

Document Type

Article

Publication Date

7-7-2015

Journal

Proceedings of the National Academy of Sciences of the United States of America

Volume

112

Issue

27

First Page

8457

Last Page

62

URL with Digital Object Identifier

10.1073/pnas.1500438112

Abstract

Anterior cingulate and lateral prefrontal cortex (ACC/PFC) are believed to coordinate activity to flexibly prioritize the processing of goal-relevant over irrelevant information. This between-area coordination may be realized by common low-frequency excitability changes synchronizing segregated high-frequency activations. We tested this coordination hypothesis by recording in macaque ACC/PFC during the covert utilization of attention cues. We found robust increases of 5-10 Hz (theta) to 35-55 Hz (gamma) phase-amplitude correlation between ACC and PFC during successful attention shifts but not before errors. Cortical sites providing theta phases (i) showed a prominent cue-induced phase reset, (ii) were more likely in ACC than PFC, and (iii) hosted neurons with burst firing events that synchronized to distant gamma activity. These findings suggest that interareal theta-gamma correlations could follow mechanistically from a cue-triggered reactivation of rule memory that synchronizes theta across ACC/PFC.