Hippocampal Respiration-Driven Rhythm Distinct from Theta Oscillations in Awake Mice

Abstract

We have recently described a slow oscillation in the hippocampus of urethane-anesthetized mice, which couples to nasal respiration and is clearly distinct from co-occurring theta oscillations. Here we set out to investigate whether such type of patterned network activity, which we named "hippocampal respiration rhythm" (HRR), also occurs in awake mice. In freely moving mice, instantaneous respiration rate is extremely variable, and respiration is superimposed by bouts of sniffing. To reduce this variability, we clamped the behavior of the animal to either awake immobility or treadmill running by using a head-fixed setup while simultaneously recording respiration and field potentials from the olfactory bulb (OB) and hippocampus. Head-fixed animals often exhibited long periods of steady respiration rate during either immobility or running, which allowed for spectral and coherence analyses with a sufficient frequency resolution to sort apart respiration and theta activities. We could thus demonstrate the existence of HRR in awake animals, namely, a respiration-entrained slow rhythm with highest amplitude at the dentate gyrus. HRR was most prominent during immobility and running with respiration rates slower than theta oscillations. Nevertheless, HRR could also be faster than theta. Discharges of juxtacellularly recorded cells in CA1 and dentate gyrus were modulated by HRR and theta oscillations. Granger directionality analysis revealed that HRR is caused by the OB and that theta oscillations in OB are caused by the hippocampus. Our results suggest that respiration-coupled oscillations aid the exchange of information between olfactory and memory networks.

Organization of prefrontal network activity by respiration-related oscillations

“…1a). In agreement with previous reports, breathing frequency was highly variable during free movement in the home cage20 (Fig. 1a).…”

“…Interestingly, hippocampal RR prominently emerges during awake immobility and entrains discharges of subpopulations of neurons, suggesting that this activity pattern may contribute to information processing in cortical neuronal circuits, especially when theta activities are weak20. On the basis of these observations, we hypothesized that RRs might functionally complement theta patterns, particularly during immobility, and play a role in the organization of prefrontal network activity.…”

“…Recently, a novel slow respiration-locked rhythm (RR) has been identified in the hippocampus181920 and barrel cortex of mice21. Interestingly, hippocampal RR prominently emerges during awake immobility and entrains discharges of subpopulations of neurons, suggesting that this activity pattern may contribute to information processing in cortical neuronal circuits, especially when theta activities are weak20.…”

Odor-Induced Neuronal Rhythms in the Olfactory Bulb Are Profoundly Modified in ob/ob Obese Mice

“…When the animal was freely exploring the arena in the absence of odorant stimulation, LFP oscillatory activity was characterized by bursts of gamma activity superimposed on slow deflections of the signal corresponding to the respiration-related rhythm (Nguyen Chi et al, 2016). We observed that this relation to respiration was preserved in ob/ob mice.…”

Breathing as a Fundamental Rhythm of Brain Function

“…Experiments in anesthetized rodents show that respiration-locked oscillations in the piriform cortex are driven this way by respiration-locked activity of olfactory bulb afferents (Fontanini and Bower, 2005; Uchida et al, 2014), which also drive respiration-locked activity in the hippocampus of mice, both under anesthesia (Yanovsky et al, 2014) and while awake and walking on a tread mill (Nguyen Chi et al, 2016). However, the mechanisms behind respiration-locked modulations of gamma power, which we observed in the mouse somatosensory cortex (Figure 1), are less obvious.…”