Organization of prefrontal network activity by respiration-related oscillations

Abstract

The medial prefrontal cortex (mPFC) integrates information from cortical and sub-cortical areas and contributes to the planning and initiation of behaviour. A potential mechanism for signal integration in the mPFC lies in the synchronization of neuronal discharges by theta (6–12 Hz) activity patterns. Here we show, using in vivo local field potential (LFP) and single-unit recordings from awake mice, that prominent oscillations in the sub-theta frequency band (1–5 Hz) emerge during awake immobility in the mPFC. These oscillation patterns are distinct from but phase-locked to hippocampal theta activity and occur synchronized with nasal respiration (hence termed prefrontal respiration rhythm [PRR]). PRR activity modulates the amplitude of prefrontal gamma rhythms with greater efficacy than theta oscillations. Furthermore, single-unit discharges of putative pyramidal cells and GABAergic interneurons are entrained by prefrontal PRR and nasal respiration. Our data thus suggest that PRR activity contributes to information processing in the prefrontal neuronal network.

Respiration-coupled rhythms in prefrontal cortex: beyond if, to when, how, and why

“…Several important reports (Tort et al 2017; Biskamp et al 2017; Zhong et al 2017) which appeared recently after our publication (Roy et al 2017) further support and clarify this interpretation. As explained by Tort et al (2017) “local generation of an oscillation is typically inferred by bipolar recordings, current source density analysis, or modulation of unit activity in the recorded region”.…”

“…This group used multi-site recordings to detect RROs in freely moving mice in 15 widespread cortical regions, including PFC, insula, parietal and visual cortices, as well as in HC, entorhinal cortex and subcortical structures such as the medio-dorsal thalamus and amygdala. In many of these structures, the local origin of RROs has been shown by current source density analysis [e.g., in HC (Lockmann et al 2016)] or rhythmic modulation of spiking [e.g., in PFC, HC (Biskamp et al 2017; Zhong et al 2017)]. Tort et al argue that as neocortical circuits are known to generate “genuine delta oscillations”, it is less likely “that all delta-frequency activity in the cortex would be due to respiration” (Tort et al 2017).…”

“…They suggest that this activity “contributes to the processing of multimodal information streams that reach the PFC from cortical and subcortical brain areas” and proposed that it “may support the synthesis of multimodal information content as a basis of decision-making and execution of certain behaviors” (Biskamp et al 2017), i.e., the primary function of PFC. They regard RROs as part of the family of sub-theta frequency activity patterns which emerge in different behaviors—including anxiety and working memory—and which may or may not synchronize with RR, depending on state.…”

“…Modulation of high frequency oscillations by slow rhythms has been proposed as a powerful mechanism of neural processing (Tort et al 2009). RROs were recently found to modulate local beta rhythms in the OB and HC (Lockmann et al 2017) and gamma rhythms in several higher brain structures (Biskamp et al 2017; Zhong et al 2017). Zhong et al (2017) specifically tested low-frequency modulation of gamma activity in OB, PFC, parietal cortex, and HC and found region- and behavior-dependent modulation of different gamma bands, i.e., modulation of 40–80 Hz gamma by theta and of 80–120 Hz gamma by RROs, “indicative of selective local computations in the respective networks” (Zhong et al 2017).…”

Nasal respiration entrains neocortical long‐range gamma coherence during wakefulness

“…This cortical respiratory potential (CRP) is lost after bulbectomy. CRPs were also observed in the dentate gyrus (Lockmann, Laplagne, Leão, & Tort, ; Nguyen‐Chi et al., ; Yanovsky, Ciatipis, Draguhn, Tort, & Branka, ), medial prefrontal (Pf), orbitofrontal cortex (Biskamp, Bartos, & Sauer, ; Kőszeghy, Lasztóczi, Forro, & Klausberger, ; Moberly et al., ; Zhong et al., ), and primary visual (V1) and motor (M1) cortex (Rojas‐Líbano, Wimmer del Solar, Aguilar‐Rivera, Montefusco‐Siegmund, & Maldonado, ) of rats and mice. Other studies have shown that CRPs are also present in several regions of the human brain (Herrero, Khuvis, Yeagle, Cerf, & Mehta, ; Zelano et al., ).…”