Breathing as a Fundamental Rhythm of Brain Function

Abstract

Ongoing fluctuations of neuronal activity have long been considered intrinsic noise that introduces unavoidable and unwanted variability into neuronal processing, which the brain eliminates by averaging across population activity (Georgopoulos et al., 1986; Lee et al., 1988; Shadlen and Newsome, 1994; Maynard et al., 1999). It is now understood, that the seemingly random fluctuations of cortical activity form highly structured patterns, including oscillations at various frequencies, that modulate evoked neuronal responses (Arieli et al., 1996; Poulet and Petersen, 2008; He, 2013) and affect sensory perception (Linkenkaer-Hansen et al., 2004; Boly et al., 2007; Sadaghiani et al., 2009; Vinnik et al., 2012; Palva et al., 2013). Ongoing cortical activity is driven by proprioceptive and interoceptive inputs. In addition, it is partially intrinsically generated in which case it may be related to mental processes (Fox and Raichle, 2007; Deco et al., 2011). Here we argue that respiration, via multiple sensory pathways, contributes a rhythmic component to the ongoing cortical activity. We suggest that this rhythmic activity modulates the temporal organization of cortical neurodynamics, thereby linking higher cortical functions to the process of breathing.

Keywords: cortical oscillations; embodied cognition; graph theory; mind-body; phase amplitude coupling; phase transitions; proprioception; respiration.

Figure 1

From Ito et al. (2014): respiratory modulation of the power of gamma frequency oscillations in mouse whisker barrel cortex. Phase–amplitude coupling between respiration-locked delta and gamma band oscillations in the barrel cortical local field potential (LFP) activity of an awake intact and an awake bulbectomized mouse, followed by population statistics. (A) Respiratory activity (top trace), amplitude of gamma band oscillations (middle trace) and delta oscillations (light green bottom trace) and its phase (dark green bottom trace) in an intact mouse. Gamma oscillation (75 Hz) amplitude peaks rhythmically phase locked to the delta cycle. (B) Gamma oscillation amplitude as a function of delta phase (red). The solid and dotted black lines indicate the mean and the 2.5 and 97.5 percentile boundaries of the surrogate amplitude distribution estimated from 1000 phase-randomized surrogates. Gamma amplitude modulation is significant at phase 0 of the delta cycle. (C,D) Same as (A,B), respectively, but for a bulbectomized mouse. After removal of the olfactory bulb, the amplitude modulation of the gamma band oscillations is no longer phase locked to respiration.

Figure 2

Results of calculations using graph theory models of coupled excitatory-inhibitory populations; the following parameter values are used: proportion of excitatory units OMEGA = 0.75, expected number of long axonal connections (shortcuts) is LAMBDA = 0.0017. (A) Phase diagram with parameter regions with the dominance of limit cycle oscillations (purple), nonzero fixed point (light green) and zero-fixed point (blue) regimes; the yellow circle corresponds to parameter settings used in (B) plot at the edge of the limit cycle regime, close the fixed point regime. (B) Illustration of the phase-locked amplitude modulation of the gamma oscillations (of excitatory population) in response to periodic input (respiration) perturbations of increasing amplitude (RA); (Ba) RA = 0.001; (Bb) RA = 0.02; (Bc) RA = 0.03; (Bd) shape of the respiratory sinusoid signal. The amplitude modulation of the inherent high-frequency oscillation (around 60 Hz) is locked to the respiratory cycle, so that the high-frequency component has increased magnitude during the increasing segment of the input signal from its minimum value.