Breathing modulates gamma synchronization across species

González, Joaquín; Cavelli, Matías; Mondino, Alejandra; Castro-Zaballa, Santiago; Brankačk, Jurij; Draguhn, Andreas; Torterolo, Pablo; Tort, Adriano Bretanha Lopes

doi:10.1007/s00424-022-02753-0

Cited by 22 publications

(16 citation statements)

References 76 publications

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“…As shown previously (Cavelli et al, 2020;González et al, 2023aGonzález et al, , 2023b, during wakefulness, a significant correlation was observed between respiration and low-gamma activity in the OB, piriform cortex and neocortical regions, which declined during sleep.…”

Section: Hfo Are Modulated By Respiration and Propagated From The Obsupporting

confidence: 84%

Cortical high-frequency oscillations (≈ 110 Hz) in cats are state-dependent and enhanced by a subanesthetic dose of ketamine

Castro

González

Cavelli

et al. 2023

Preprint

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Ketamine is an NMDA receptor antagonist that has both antidepressant and anesthetic properties. At subanesthetic doses, ketamine can cause transient psychosis in humans, and is used to model psychosis in experimental animals. In rodents, subanesthetic doses of ketamine increase the power of high-frequency oscillations (HFO, 100-180 Hz) in the electroencephalogram and field potentials, a frequency band linked to cognitive functions. However, the effects of ketamine in higher mammals, with more translatable relevance, are poorly investigated. Here, we have examined cortical HFO during wakefulness, sleep, and after administering a sub-anesthetic dose of ketamine (15 mg/kg), utilizing the cat as an animal model. Four cats were implanted with cortical electrodes for chronic polysomnographic recordings. HFO power, connectivity, information flow directionality, and their relationships with respiratory activity were analyzed. During wakefulness, but not during sleep, we found that HFO were coupled with the inspiratory phase of the respiration. After ketamine administration, HFO were enhanced significantly and remained associated with the inspiratory phase. The analysis of the information flow after ketamine suggest that HFO originate from the olfactory bulb and stream towards the prefrontal cortex. Accordingly, occluding the nostrils significantly reduced HFO power in both the olfactory bulb and prefrontal cortex. In contrast, auditory stimulation did not affect HFO. In conclusion, spontaneous cortical HFO show certain state-dependent features in cats, and enhancement of this rhythm by ketamine may disrupt cortical information processing, which could contribute to some of the neuropsychiatric manifestations associated with ketamine.

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Section: Hfo Are Modulated By Respiration and Propagated From The Obsupporting

confidence: 84%

Cortical high-frequency oscillations (≈ 110 Hz) in cats are state-dependent and enhanced by a subanesthetic dose of ketamine

Castro

González

Cavelli

et al. 2023

Preprint

Self Cite

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“…Notably, these authors also found that inhibitory recruitment by assembly members was key for assembly segregation, suggesting a potential role for gamma in that area. Hence, the directional view of synchronization across regions places a major role in cross-frequency interactions driving communication, highlighting the relevance of interregional synchrony modulation by slower rhythms, for instance, theta ( González et al, 2020 ) or respiration itself ( Cavelli et al, 2020 ; González et al, 2023 ).…”

Section: Discussionmentioning

confidence: 99%

Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex

González

Torterolo

Tort

2023

eLife

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Gamma oscillations are believed to underlie cognitive processes by shaping the formation of transient neuronal partnerships on a millisecond scale. These oscillations are coupled to the phase of breathing cycles in several brain areas, possibly reflecting local computations driven by sensory inputs sampled at each breath. Here, we investigated the mechanisms and functions of gamma oscillations in the piriform (olfactory) cortex of awake mice to understand their dependence on breathing and how they relate to local spiking activity. Mechanistically, we find that respiration drives gamma oscillations in the piriform cortex, which correlate with local feedback inhibition and result from recurrent connections between local excitatory and inhibitory neuronal populations. Moreover, respiration-driven gamma oscillations are triggered by the activation of mitral/tufted cells in the olfactory bulb and are abolished during ketamine/xylazine anesthesia. Functionally, we demonstrate that they locally segregate neuronal assemblies through a winner-take-all computation leading to sparse odor coding during each breathing cycle. Our results shed new light on the mechanisms of gamma oscillations, bridging computation, cognition and physiology.

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“…To examine the relationships between two oscillators at different speeds, researchers analyze how the phase of the slower oscillator relates to the phase, frequency, or amplitude of faster ones [40][41][42] . Ito et al, 2014 provided evidence using mice for cross-frequency coupling between breathing and brain time series.…”

Section: Brain-breathing Cross-frequency Couplingmentioning

confidence: 99%

Dynamic Mechanisms That Couple the Brain and Breathing to the External Environment

Goheen,

Wolman,

Angeletti

et al. 2023

Preprint

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Brain and breathing activity are closely linked to each other. For instance, oscillations in breathing have been causally linked to oscillations in arousal and cognition. However, the exact neurophysiological mechanisms of brain breathing coupling are not yet agreed upon. In this perspective, we highlight two key dynamic mechanisms, namely brain breathing synchronization and dynamic attunement of both brain and breathing to external periodic stimuli. First, we review the existing literature which provides strong evidence for the synchronization of brain and breathing in terms of coherence, cross-frequency coupling, and phase-based entrainment. Second, using preliminary EEG and breathing data, we show that both lungs and brain attune the temporal structure of their power spectra to the periodic structure of external inputs. We highlight the key role of two dynamic mechanisms, synchronization and attunement, in coordinating the tripartite temporal alignment of the brain, breathing and their input dynamics. We conclude that the three different systems of brain, lungs and environment are directly connected through shared dynamics as their “common currency”1,2. Our research does not only shed light on the dynamic mechanisms of brain-breathing coupling but also carries major clinical and therapeutic implications concerning conditions where the adaptability of brain and breathing systems is compromised for instance in psychiatric illness or cognitive aging.

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Breathing modulates gamma synchronization across species

Cited by 22 publications

References 76 publications

Cortical high-frequency oscillations (≈ 110 Hz) in cats are state-dependent and enhanced by a subanesthetic dose of ketamine

Cortical high-frequency oscillations (≈ 110 Hz) in cats are state-dependent and enhanced by a subanesthetic dose of ketamine

Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex

Dynamic Mechanisms That Couple the Brain and Breathing to the External Environment

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