Respiratory Rhythms of the Predictive Mind

Abstract

All living organisms breathe. Respiratory rhythms sustain biological life, governing the homeostatic exchange of oxygen and carbon dioxide. Until recently however, the influence of breathing on the brain has largely been overlooked. Yet new evidence demonstrates that respiratory rhythms exert surprising, substantive influences on perception, emotion, and cognition, largely through the direct modulation of neural oscillations. Here we synthesize these findings to motivate a new predictive coding model of respiratory brain coupling, in which the breath rhythmically enhances both local and global neural gain, to optimize cognitive and affective processing. Our model further explains how respiratory rhythms interact with the topology of the functional connectome, and we highlight key implications for the computational psychiatry of disordered respiratory and interoceptive inference.

Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling

“…A second hypothesis would be that periodic and aperiodic changes reflect modulation of two different respiration-related pathways: As outlined above, while the respiratory rhythm itself is generated in the brain stem 45 , oscillatory changes are assumed to be induced by mechanosensory stimulation from the nasal airstream during inspiration and expiration. In their predictive coding model of respiratory interoception, Allen and colleagues 46 recently proposed a deep control circuit of respiratory nuclei within the brainstem to monitor ascending breath-by-breath dynamics sent via the vagus nerve. These signals are thought to serve the longer-term maintenance of homeostatic parameters like respiratory frequency and CO 2 levels.…”

Brain-heart interactions are optimized across the respiratory cycle via interoceptive attention

“…A third intriguing explanation of our results relies on the predictive coding model of interoceptive perception (Barrett and Simmons, 2015; Seth, 2013; Seth and Friston, 2016). In brief, recent interoceptive inference models (Allen et al, 2019; Allen et al, 2021) posit that cardiorespiratory interoception is able to shape the neural gain (i.e., the balance of neural excitation vs. inhibition) across several brain regions by modulating the computational precision (i.e., the inverse of noise) of perceptual, cognitive, and emotional processes. More in detail, periodic physiological changes related to rhythmic cardiorespiratory oscillations are computed by the brain as stable predictions and are centrally suppressed via a sensory attenuation process in order to minimize their interference.…”

“…Hence, the question arises of why we observed different respiratory phase-dependent modulations of HEP activity between the IC (higher ΔHEP) and the EC (lower ΔHEP). According to the above-described interoceptive inference models (Allen et al, 2019; Allen et al, 2021), interoceptive prediction is not an all-or-none phenomenon, but a highly context-sensitive process determining the precision of incoming sensations based on the ongoing task-oriented cognition. Therefore, during the IC, to be able to correctly perceive and process heartbeat sensations across the respiratory cycle, the brain may adaptively increase the precision of interoceptive cardiac input specifically during exhalations, that is, when inhalation-related physiological noise is absent.…”

“…Differently, self-initiated motor actions (Park et al, 2020), and trace eyeblink conditioning learning (Waselius et al, 2019) were more frequent during exhalation, while the exhalation-to-inhalation phase transition improved recognition memory performance (Nakamura et al, 2018). Based on this and other evidence, within the framework of predictive coding theories of brain functioning (Clark, 2013; Friston, 2010), respiration has been recently interpreted as a form of “active sensing” (Allen et al, 2021; Boyadzhieva and Kayhan, 2021; Corcoran et al, 2018): that is, spontaneous inhalation may adaptively modulate cortical excitability to facilitate reception and elaboration of incoming sensory information from the environment, namely, exteroceptive information (Tort et al, 2018). Hence, the question arises of whether spontaneous respiration plays a role in shaping the processing of interoceptive information generated from inside the body as well.…”

The Respiratory Resistance Sensitivity Task: An Automated Method for Quantifying Respiratory Interoception and Metacognition

“…Our results show that the RRST provides highly reliable measurement of respiroceptive thresholds in just 20-30 minutes, and is minimally aversive for participants. Further, by enabling the rapid collection of many near-threshold trials in a 2IFC design, the RRST can flexibly dissociate interoceptive sensitivity, precision, and bias, and is well suited for model-based research in interoceptive perceptual decision-making over both perceptual and metacognitive dimensions (see e.g., (Allen et al, 2021;Allen, Levy, et al, 2019;Unal et al, 2021).…”