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Respiration aligns perception with neural excitability.

ABSTRACT: Recent studies from the field of interoception have highlighted the link between bodily and neural rhythms during action, perception, and cognition. The mechanisms underlying functional body-brain coupling, however, are poorly understood, as are the ways in which they modulate behavior. We acquired respiration and human magnetoencephalography data from a near-threshold spatial detection task to investigate the trivariate relationship between respiration, neural excitability, and performance. Respiration was found to significantly modulate perceptual sensitivity as well as posterior alpha power (8-13 Hz), a well-established proxy of cortical excitability. In turn, alpha suppression prior to detected versus undetected targets underscored the behavioral benefits of heightened excitability. Notably, respiration-locked excitability changes were maximized at a respiration phase lag of around -30° and thus temporally preceded performance changes. In line with interoceptive inference accounts, these results suggest that respiration actively aligns sampling of sensory information with transient cycles of heightened excitability to facilitate performance.

SUBMITTER: Kluger DS

PROVIDER: S-EPMC8763394 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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Respiration aligns perception with neural excitability.

Kluger Daniel S DS Balestrieri Elio E Busch Niko A NA Gross Joachim J

eLife 20211214

Recent studies from the field of interoception have highlighted the link between bodily and neural rhythms during action, perception, and cognition. The mechanisms underlying functional body-brain coupling, however, are poorly understood, as are the ways in which they modulate behavior. We acquired respiration and human magnetoencephalography data from a near-threshold spatial detection task to investigate the trivariate relationship between respiration, neural excitability, and performance. Res ...[more]

PMID: 34904567

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Project description:The relationship between macroscale electrophysiological recordings and the dynamics of underlying neural activity remains unclear. We have previously shown that low frequency EEG activity (<1 Hz) is decreased at the seizure onset zone (SOZ), while higher frequency activity (1-50 Hz) is increased. These changes result in power spectral densities (PSDs) with flattened slopes near the SOZ, which are assumed to be areas of increased excitability. We wanted to understand possible mechanisms underlying PSD changes in brain regions of increased excitability. We hypothesized that these observations are consistent with changes in adaptation within the neural circuit. We developed a theoretical framework and tested the effect of adaptation mechanisms, such as spike frequency adaptation and synaptic depression, on excitability and PSDs using filter-based neural mass models and conductance-based models. We compared the contribution of single timescale adaptation and multiple timescale adaptation. We found that adaptation with multiple timescales alters the PSDs. Multiple timescales of adaptation can approximate fractional dynamics, a form of calculus related to power laws, history dependence, and non-integer order derivatives. Coupled with input changes, these dynamics changed circuit responses in unexpected ways. Increased input without synaptic depression increases broadband power. However, increased input with synaptic depression may decrease power. The effects of adaptation were most pronounced for low frequency activity (< 1Hz). Increased input combined with a loss of adaptation yielded reduced low frequency activity and increased higher frequency activity, consistent with clinical EEG observations from SOZs. Spike frequency adaptation and synaptic depression, two forms of multiple timescale adaptation, affect low frequency EEG and the slope of PSDs. These neural mechanisms may underlie changes in EEG activity near the SOZ and relate to neural hyperexcitability. Neural adaptation may be evident in macroscale electrophysiological recordings and provide a window to understanding neural circuit excitability.

Dataset Information

Respiration aligns perception with neural excitability.

Publications

Respiration aligns perception with neural excitability.

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