Respiration-Driven Brain Oscillations in Emotional Cognition

Abstract

Respiration paces brain oscillations and the firing of individual neurons, revealing a profound impact of rhythmic breathing on brain activity. Intriguingly, respiration-driven entrainment of neural activity occurs in a variety of cortical areas, including those involved in higher cognitive functions such as associative neocortical regions and the hippocampus. Here we review recent findings of respiration-entrained brain activity with a particular focus on emotional cognition. We summarize studies from different brain areas involved in emotional behavior such as fear, despair, and motivation, and compile findings of respiration-driven activities across species. Furthermore, we discuss the proposed cellular and network mechanisms by which cortical circuits are entrained by respiration. The emerging synthesis from a large body of literature suggests that the impact of respiration on brain function is widespread across the brain and highly relevant for distinct cognitive functions. These intricate links between respiration and cognitive processes call for mechanistic studies of the role of rhythmic breathing as a timing signal for brain activity.

Keywords: embodied cognition; emotion; network; neuronal circuits; neuronal synchronization; oscillations; respiration; slow oscillation.

Figure 1

Respiration-driven slow oscillations are widespread in the cortex. (A) Top, black: respiratory trace measured with a thermistor. Bottom, red/blue: LFP traces from two recording sites located 300 μm apart in the whisker barrel cortex during accelerated breathing induced by exposure to hypoxic air. Reprinted from Ito et al. (2014) under CC BY 4.0. (B) Video-based measuring of breathing (BRE signal, top) and simultaneous LFP recordings from OFC, OB, and hippocampus (HIP) during immobility. Reprinted from Kőszeghy et al. (2018) under CC BY 4.0. (C) Top, blue: respiration trace measured with a thermocouple. Middle and bottom, black: simultaneous LFP recordings from the OB and dentate gyrus (DG) of the hippocampus. Reprinted from Nguyen Chi et al. (2016) under CC BY 4.0. (D) The mPFC shows strong entrainment by respiration across a variety of behavioral states. Top: mPFC LFP recorded during immobility during the tail suspension test. Bottom: The simultaneous respiratory trace measured with a thermocouple. Adapted from Biskamp et al. (2017) under CC BY 4.0. Bottom: Synchronous LFP signal from the OB and prelimbic cortex (plPFC) recorded during auditory fear conditioning. Please note the increase in the amplitude of the 4 Hz rhythm in both LFP signals at freezing onset, indicated by the horizontal blue bar. Adapted from Moberly et al. (2018) under CC BY 4.0. *p < 0.05.

Figure 2

The generation and propagation of respiration-related oscillations in the brain. Rhythmic breathing is generated in the brain stem and feeds back onto neocortical and hippocampal circuits via nasal airflow (red): Air movement through the nasal cavity excites OSNs, which transmit this rhythmic input to mitral and tufted cells of the OB. Via the olfactory cortex, RR reaches the neocortex and subcortical structures. In a presumed corollary discharge pathway, brain stem signals might in addition directly impose RR on cortical circuits (black).

Figure 3

Modulation of fear-related neural correlates and recognition of fearful faces by respiration. (A) The mPFC is entrained at 4 Hz by RR sensorial afferences during freezing. Spectrogram averaged across mice at freezing onset and offset, indicated by the white vertical dashed lines. Power spectra of the OB (top) and medial prefrontal cortex (PFC, middle) of control mice. Bottom: Power spectrum of the PFC of mice after bulbectomy. Reprinted from Bagur et al. (2021) under CC BY 4.0. (B) The mPFC and the basolateral amygdala (BLA) are highly coherent at 4 Hz during freezing. Top: Bandpass filtered 2–6 Hz LFP signals of the mPFC (black) and the simultaneously recorded BLA LFP (blue) during recall of conditioned fear. Freezing epochs are indicated by the horizontal black lines. Bottom: Phase difference between the mPFC and the amygdala (Red: above 0° of phase difference, mPFC phase precedes BLA phase. Blue: Below 360°, BLA phase precedes mPFC phase. Gray: simulated phase differences obtained by bootstrapping). Adapted by permission from Springer Nature, Nature Neuroscience, Karalis et al. (2016), copyright (2016). (C) The periamygdaloid cortex receives direct projection from the OB. BLA units are furthermore paced by RR in the home cage (Karalis and Sirota, 2018). (D) Inspiration facilitates the recognition of fearful faces. Top right, experimental paradigm: subjects had to discriminate between fearful or surprised faces presented at jittering interval of 2–5 s during nasal or oral breathing (gray line). Middle left: reaction time to recognize expressions for each emotion (yellow: fear, blue: surprise), depending on the phase of respiration (full: inspiration, dashed: expiration) and the breathing route. Middle right: Detrended reaction time for the recognition of fear for four phases of the breathing cycle. Oral breathing induced an increase in the reaction time during late inspiration. Bottom: Correlation between reaction time and the mean z-scored power in the delta band during the whole inspiration or expiration time window. On the left, “Fear inhale” shows the results for fearful faces presented during inspiration, and “Fear exhale” the results for fearful faces presented during expiration. Reprinted from Zelano et al. (2016) under CC BY 4.0. *p < 0.05.

Figure 4

The reward system and respiration-related oscillations. (A) Topography of the projections from the frontal cortex to the striatum. The olfactory tubercle (OT) receives direct projections from the OB and the nucleus accumbens (NAcc) has been shown to be strongly entrained by RR (Karalis and Sirota, 2018). In the prefrontal cortex, the RR power increases from dorsal to ventral (Karalis and Sirota, ; Folschweiller and Sauer, 2021). Adapted from Voorn et al. (2004), copyright (2004) Trends in Neurosciences, with permission from Elsevier. (B) Left: Power spectra of the mPFC along the dorsoventral axis, shows an increase in power at the frequency of respiration in the ventral direction. Left: Peak power for each mouse at 4 Hz at the most superficial recording site (light blue) and the deepest recording site (dark blue) of the mPFC. Reprinted from Folschweiller and Sauer (2021) under CC BY 4.0. *p < 0.05.

Figure 5

Mechanisms of how breathing might impact cognition. (A) Left: RR entrains fast gamma activities across brain circuits. PLC, prelimbic cortex; PAC, parietal cortex. Reprinted from Zhong et al. (2017). Right: Respiration and theta oscillations provide timing signals for gamma oscillations of different frequencies (Biskamp et al., ; Zhong et al., 2017). (B) Left: Respiration paces ripples. Top: Example of a hippocampal ripple. Bottom: Average ripple power spectrum (left) and distribution of ripple events as a function of respiration phase. Reprinted from Liu et al. (2017) under CC BY 4.0. Right: RR-entrained ripples might enable efficient communication between hippocampal and neocortical circuits (Liu et al., ; Karalis and Sirota, 2018). (C) Top: Neuronal assemblies activate during the descending part of the prefrontal respiration-related oscillation (RRO). Reprinted from Folschweiller and Sauer (2021) under CC BY 4.0. Bottom: RR creates time windows for assembly activation and might thus orchestrate the joint activity of distributed assembly members or facilitate assembly stabilization by offline reactivation (Dejean et al., ; Folschweiller and Sauer, 2021).