Theta/delta coupling across cortical laminae contributes to semantic cognition

Adams, Natalie E., Teige, Catarina, Mollo, Giovanna, Karapanagiotidis, Theodoros, Cornelissen, Piers, Smallwood, Jonathan, Traub, Roger D., Jefferies, Elizabeth and Whittington, Miles A. (2019) Theta/delta coupling across cortical laminae contributes to semantic cognition. Journal of Neurophysiology, 121 (4). pp. 1150-1161. ISSN 0022-3077

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Abstract

Rhythmic activity in populations of neurons is associated with cognitive and motor function. Our understanding of the neuronal mechanisms underlying these core brain functions has benefitted from demonstrations of cellular, synaptic and network phenomena leading to the generation of discrete rhythms at the local network level. However, discrete frequencies of rhythmic activity rarely occur alone. Despite this, little is known about why multiple rhythms are generated together or what mechanisms underlie their interaction to promote brain function. One overarching theory is that different temporal scales of rhythmic activity correspond to communication between brain regions separated by different spatial scales. To test this we quantified the cross-frequency interactions between two dominant rhythms – theta and delta activity - manifest during MEG recordings of subjects performing a word-pair semantic decision task. Semantic processing has been suggested to involve the formation of functional links between anatomically disparate neuronal populations over a range of spatial scales and a distributed network was manifest in the profile of theta-delta coupling seen. Furthermore, differences in the pattern of theta-delta coupling significantly correlated with semantic outcome. Using an established experimental model of concurrent delta and theta rhythms in neocortex we show that these outcome-dependent dynamics could be reproduced in a manner determined by the strength of cholinergic neuromodulation. Theta-delta coupling correlated with discrete neuronal activity motifs segregated by cortical layer, neuronal intrinsic properties and long range axonal targets. Thus, the model suggested that local, interlaminar neocortical theta-delta coupling may serve to coordinate both cortico-cortical and cortico-subcortical computations during distributed network activity.

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