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-manifested during magnetoencephalography 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 the 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. NEW & NOTEWORTHY Here, we show, for the first time, that a network of spatially distributed brain regions can be revealed by cross-frequency coupling between delta and theta frequencies in subjects using magnetoencephalography recording during a semantic decision task. A biological model of this cross-frequency coupling suggested an interlaminar, cell-specific division of labor within the neocortex may serve to route the flow of cortico-cortical and cortico-subcortical information to promote such spatially distributed, functional networks.
Highlights
Rhythmic electrical activity in discrete frequency bands accompanies a broad range of motor, affective, and cognitive processes in the brain
Gamma rhythms organize primary sensory information to facilitate higher-order processing (Fries 2015); beta rhythm generation correlates with task performance, requiring short-term memory and prediction (Arnal and Giraud 2012); alpha rhythms control access to stored memories (Klimesch 2012); theta rhythms appear to be required for sequential processing of sensory information (Remondes and Wilson 2013); delta rhythms appear vital for semantic processing (Harmony 2013)
We examined any relationship between the theta rhythmic activity and the other dominant component of the spectra revealed in Fig. 3A—the delta rhythm
Summary
Rhythmic electrical activity in discrete frequency bands accompanies a broad range of motor, affective, and cognitive processes in the brain. Where the information is available, these rhythms appear to have an origin in subsets of neurons in local cortical and thalamic circuits (Roopun et al 2008), but the temporal organization they impart onto local circuit outputs is vital for control of information flow within the wider cortical mantle (e.g., Akam and Kullmann 2010; Li et al 2017). Coexistence of multiple frequencies of activity, each temporally interacting with one another, is a common feature of brain dynamics (Lakatos et al 2005), but we understand little about the mechanisms that facilitate these interactions, nor the computational advantages they may impart: Do they just represent a simple additive process, with one brain region involved simultaneously in multiple cortical processes, or is there synergy at work, with the presence of multiple, interacting rhythms superadditive for cortical function? Coexistence of multiple frequencies of activity, each temporally interacting with one another, is a common feature of brain dynamics (Lakatos et al 2005), but we understand little about the mechanisms that facilitate these interactions, nor the computational advantages they may impart: Do they just represent a simple additive process, with one brain region involved simultaneously in multiple cortical processes, or is there synergy at work, with the presence of multiple, interacting rhythms superadditive for cortical function? There is increasing evidence for the latter, leading to the current working hypothesis that different frequencies of rhythm chaperone cortical communication on different spatial scales (Canolty and Knight 2010; Kopell et al 2000)
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