Rhythms are ubiquitous in nature. Brain rhythms coordinate large populations of neurons within and between different brain regions. The respiratory rhythm is an ongoing process controlled by brainstem networks. Olfaction depends on respiration at a fundamental level, as do the robust neural oscillations generated by the olfactory system that are important for perception and learning. More centrally, hippocampal circuits, which receive input from all sensory modalities and most directly from the olfactory system, are a major generator of brain rhythms important for spatial navigation and learning. Recent studies in rodents and humans have shown neural oscillations in prefrontal, limbic, primary sensory and motor areas phase-locked simultaneously to both the respiratory and hippocampal theta rhythms. Rodents breathe faster than humans at a frequency (~2-12 Hz) that overlaps with hippocampal theta oscillations (4-12 Hz). This suggests previous studies on hippocampal functioning may have overlooked, due to lack of respiratory recordings, roles of the respiratory rhythm, similar to those of hippocampal theta, in coordinating activity for spatial memory processes. Here, we characterize dynamic respiratory and theta network configurations depending on the perceptual environment during spatial navigation and learning. In the first set of experiments, local field potentials (LFPs) were recorded in olfactory areas including the olfactory bulb (OB) and piriform cortex (PC), along with CA1 and dentate gyrus of the hippocampus, and the primary visual cortex, simultaneously with nasal respiratory recordings during spatial navigation in rats. We compared interactions among these areas while rats foraged using either visual or olfactory spatial cues and found high coherence during foraging in both modalities compared to home cage activity in two frequency bands that matched slow and fast respiratory rates. Directional analysis shows stronger interactions between primary sensory areas relevant to the sensory modality of the foraging environment. We provide the first evidence of respiratory-OB-PC-hippocampal interactions in awake freely moving rats, supporting the theory that the PC promotes widespread respiratory coherence. In the second set of experiments, half of the rats from the first experiment were used along with another set of rats in which we also recorded from primary somatosensory (S1), secondary motor (M2), medial parietal association (mPtA), and entorhinal (EC) cortices. All rats were trained on a spatial learning task in which they had to navigate to a learned location using either visual or olfactory cues. We compared measures of neural interaction dependent on modality of spatial cues and naïve versus learned states. High levels of coherence were seen between limbic system and sensory cortices at a single frequency around hippocampal theta (~7-8 Hz). In the third study we applied phase amplitude coupling analyses to assess the modulation of faster oscillations, which represent more local activity, by the slower respiratory and theta rhythms. High gamma (60-100 Hz) amplitude was modulated by respiratory and theta rhythms in several areas during foraging and spatial learning. Primary sensory areas and the hippocampus show increased modulation of gamma amplitude by respiratory and theta phase during spatial learning. Our results support the hypothesis that respiration works dynamically with hippocampal theta as part of a master clock for global brain connectivity and help to characterize the role of these coordinated rhythms in cognitive behaviors.




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