Respiration-driven oscillations in emotional behaviour
Final Report Abstract
Respiration-rhythmic oscillations in the local field potential (LFP) emerge in the medial prefrontal cortex (mPFC), a cortical region with a key role in the regulation of emotional behaviour. Here, we examined the respiration entrainment of mouse mPFC LFP and spiking activity during states with similar behaviour (i.e., immobility) but distinct emotional valence: during awake immobility in the home cage (HC, ‘neutral’), during passive coping in response to inescapable stress under tail suspension (TS, ‘negative valence’), and during reward consumption (Rew, ‘positive valence’). We found that neuronal spikes of pyramidal cells and putative interneurons (pINs) showed significant respiration phase-coupling throughout behaviours with characteristic phase preferences depending on the behavioural state. Moreover, while phase-coupling dominated in deep layers in HC and Rew conditions, TS resulted in the recruitment of superficial layer neurons to respiration. These results jointly suggest that respiration dynamically entrains prefrontal neuronal activity depending on the emotional context. In a complementary approach focusing on population activity patterns during spontaneous immobility, we found that the activation of neuronal assemblies, that is groups of coactive pyramidal cells, is biased towards the descending phase of prefrontal respiration-related oscillations (RROs). PINs coactivate with assemblies and receive enhanced excitatory drive from assembly neurons during descending RRO, suggesting that the phase-specific recruitment of pINs might help to keep the activation of different assemblies separated from each other during times of preferred assembly activation. Taken together, our results provide key insights into how respiration modulates the activity of prefrontal neurons in a behavioural state-dependent manner and identify respiration-synchronized brain rhythms as a control element that defines time windows of enhanced assembly activity.
Publications
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Respiration-Driven Brain Oscillations in Emotional Cognition. Frontiers in Neural Circuits, 15 (2021, 10, 27).
Folschweiller, Shani & Sauer, Jonas-Frederic
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Author response: Disrupted-in-schizophrenia-1 is required for normal pyramidal cell–interneuron communication and assembly dynamics in the prefrontal cortex. (2022, 8, 26). American Geophysical Union (AGU).
Sauer, Jonas-Frederic & Bartos, Marlene
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Controlling neuronal assemblies: a fundamental function of respiration-related brain oscillations in neuronal networks. Pflügers Archiv - European Journal of Physiology, 475(1), 13-21.
Folschweiller, Shani & Sauer, Jonas-Frederic
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Phase‐specific pooling of sparse assembly activity by respiration‐related brain oscillations. The Journal of Physiology, 600(8), 1991-2011.
Folschweiller, Shani & Sauer, Jonas‐Frederic
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Topographically organized representation of space and context in the medial prefrontal cortex. Proceedings of the National Academy of Sciences, 119(6).
Sauer, Jonas-Frederic; Folschweiller, Shani & Bartos, Marlene
