Olfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior

Moberly, Andrew H.; Schreck, Mary; Bhattarai, Janardhan P.; Zweifel, Larry S.; Luo, Wenqin; Ma, Minghong

doi:10.1038/s41467-018-03988-1

Cited by 135 publications

(180 citation statements)

References 59 publications

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“…This was supported by our finding that strong correlations of BFCNREG and auditory population activities in a specific task phase was predictive of mouse performance ( Fig.6), suggesting that behavior-dependent synchronization may underlie efficient bottom-up information transfer ( Fig.8D-E). Similar to this result, careful analysis of behavior-dependent frequency coupling lead to new insight in the active sensing field by revealing behavior-dependent theta-frequency synchronization among hippocampus, respiratory and whisking circuits [69][70][71][72] and prefrontal cortex, suggesting that such theta-frequency binding might be a rather general mechanism.…”

Section: Discussionsupporting

confidence: 55%

Distinct synchronization, cortical coupling and behavioural function of two basal forebrain cholinergic neuron types

Laszlovszky

Schlingloff

Freund

et al. 2019

Preprint

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Basal forebrain cholinergic neurons (BFCN) densely innervate the forebrain and modulate synaptic plasticity, cortical processing, brain states and oscillations. However, little is known about the functional diversity of cholinergic neurons and whether distinct types support different functions. To examine this question we recorded BFCN in vivo, to examine their behavioral functions, and in vitro, to study their intrinsic properties. We identified two distinct types of BFCN that markedly differ in their firing modes, synchronization properties and behavioral correlates. Bursting cholinergic neurons (BFCNBURST) fired in zero-lag synchrony with each other, phase-locked to cortical theta activity and fired precisely timed bursts of action potentials after reward and punishment. Regular firing cholinergic neurons (BFCNREG) were found predominantly in the posterior basal forebrain, displayed strong theta rhythmicity (5-10 Hz), fired asynchronously with each other and responded with precise single spikes after behavioral outcomes. In an auditory detection task, synchronization of BFCNBURST neurons to auditory cortex predicted the timing of mouse responses, whereas tone-evoked cortical coupling of BFCNREG predicted correct detections. We propose that cortical activation relevant for behavior is controlled by the balance of two cholinergic cell types, where the precise proportion of the strongly activating BFCNBURST follows an anatomical gradient along the antero-posterior axis of the basal forebrain.

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Section: Discussionsupporting

confidence: 55%

Distinct synchronization, cortical coupling and behavioural function of two basal forebrain cholinergic neuron types

Laszlovszky

Schlingloff

Freund

et al. 2019

Preprint

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“…Finally, circular distribution analysis of the phase differences between the OB and the neocortical electrodes exhibits phase differences other than 0° or 180° (Figure S2), suggesting that CRPs were not a result of volume conduction from the OB (Moberly et al., ).…”

Section: Resultsmentioning

confidence: 99%

“…As shown in Figure 1e, the coherence between respiration and ECoG that is observed during nasal respiration in W drops during mouth breathing (two-tailed t test, p = .0001). Finally, circular distribution analysis of the phase differences between the OB and the neocortical electrodes exhibits phase differences other than 0° or 180° ( Figure S2), suggesting that CRPs were not a result of volume conduction from the OB (Moberly et al, 2018). Figure 2a shows two examples of sleep to W transitions.…”

Section: Cortical Respiratory Potentials Are Present During Wakefulmentioning

confidence: 98%

“…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., ).…”

Section: Introductionmentioning

confidence: 99%

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Nasal respiration entrains neocortical long‐range gamma coherence during wakefulness

Cavelli

Castro-Zaballa

González

et al. 2019

Eur J of Neuroscience

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Recent studies have shown that slow cortical potentials in archi‐, paleo‐ and neocortex can phase‐lock with nasal respiration. In some of these areas, gamma activity (γ: 30–100 Hz) is also coupled to the animal's respiration. It has been hypothesized that these functional relationships play a role in coordinating distributed neural activity. In a similar way, inter‐cortical interactions at γ frequency have also been associated as a binding mechanism by which the brain generates temporary opportunities necessary for implementing cognitive functions. The aim of the present study is to explore whether nasal respiration entrains inter‐cortical functional interactions at γ frequency during both wakefulness and sleep. Six adult cats chronically prepared for electrographic recordings were employed in this study. Our results show that during wakefulness, slow cortical respiratory potentials are present in the olfactory bulb and several areas of the neocortex. We also found that these areas exhibit cross‐frequency coupling between respiratory phase and γ oscillation amplitude. We demonstrate that respiratory phase modulates the inter‐cortical gamma coherence between neocortical electrode pairs. On the contrary, slow respiratory oscillation and γ cortical oscillatory entrainments disappear during non‐rapid eye movement and rapid eye movement sleep. These results suggest that a single unified phenomenon involves cross‐frequency coupling and long‐range γ coherence across the neocortex. This fact could be related to the temporal binding process necessary for cognitive functions during wakefulness.

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“…Importantly, this slow oscillation is distinct from the theta rhythm and predicts the onset and offset of freezing. Interestingly, recent work has shown that freezing-related 4Hz oscillation in the mPFC was correlated with the animal's respiratory rate, and that disruption of olfactory inputs to the mPFC significantly reduces the 4-Hz oscillation in the mPFC (Moberly et al, 2018). These data bring further support to the growing body of evidence showing that in addition to its impact on olfactory regions (for a review see Buonviso et al, 2006), nasal respiration also entrains oscillations in widespread brain regions including those involved in the fear network like the mPFC and amygdala (for a review see .…”

Section: Introductionmentioning

confidence: 99%

New insights from 22-kHz ultrasonic vocalizations to characterize fear responses: relationship with respiration and brain oscillatory dynamics

Dupin

Garcia

Boulanger-Bertolus

et al. 2018

Preprint

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Fear behavior depends on interactions between the medial prefrontal cortex (mPFC) and the basolateral amygdala (BLA), and the expression of fear involves synchronized activity in theta and gamma oscillatory activities. In addition, freezing, the most classical measure of fear response in rodents, temporally coincides with the development of sustained 4-Hz oscillations in prefrontalamygdala circuits. Interestingly, these oscillations were recently shown to depend on the animal's respiratory rhythm, supporting the growing body of evidence pinpointing the influence of nasal breathing on brain rhythms. During fearful states, rats also emit 22-kHz ultrasonic vocalizations (USV) which drastically affect respiratory rhythm. However, the relationship between 22-kHz USV, respiration and brain oscillatory activities is still unknown. Yet such information is crucial for a comprehensive understanding of how the different components of fear response collectively modulate rat's brain neural dynamics. Here we trained male rats in an odor fear conditioning task, while recording simultaneously local field potentials in BLA, mPFC and olfactory piriform cortex, together with USV calls and respiration. We show that USV calls coincide with an increase in delta and gamma power and a decrease in theta power. In addition, during USV emission in contrast to silent freezing, there is no coupling between respiratory rate and delta frequency, and the modulation of fast oscillations amplitude relative to the phase of respiration is modified. We propose that sequences of USV calls could result in a differential gating of information within the network of structures sustaining fear behavior, thus potentially modulating fear expression/memory. Significance StatementWhile freezing is the most frequently used measure of fear, it is only one amongst the different components of rodents' response to threatening events. USV is another index that gives additional insight into the socioemotional status of an individual. Our study is the first to describe the effects of USV production on rat's brain oscillatory activities in the fear neural network, and to relate some of them to changes in nasal breathing. A better knowledge of the impact of USV calls on brain neural dynamics is not only important for understanding the respective weight of the different components of fear response, but is also particularly relevant for rodent models of human neuropsychiatric disorders, for which socio-affective communication is severely impaired.

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Olfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior

Cited by 135 publications

References 59 publications

Distinct synchronization, cortical coupling and behavioural function of two basal forebrain cholinergic neuron types

Distinct synchronization, cortical coupling and behavioural function of two basal forebrain cholinergic neuron types

Nasal respiration entrains neocortical long‐range gamma coherence during wakefulness

New insights from 22-kHz ultrasonic vocalizations to characterize fear responses: relationship with respiration and brain oscillatory dynamics

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