Dissociation of fear initiation and maintenance by breathing-driven prefrontal oscillations

Bagur, Sophie; Lefort, Julie; Lacroix, Marie; Lavilléon, Gaëtan de; Herry, Cyril; Billand, Clara; Geoffroy, H; Benchenane, Karim

doi:10.1101/468264

Cited by 11 publications

(11 citation statements)

References 46 publications

(19 reference statements)

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“…Our results indicating a role for 4 Hz BLA-mPFC oscillations in stabilizing freezing bouts adds to recent reports of a respiration-synchronized 4 Hz mPFC oscillation that can similarly stabilize freezing behavior [53][54][55][56] . Based on these multiple lines of studies, we may attempt to build a general framework wherein 4 Hz respiration-synchronized oscillations can entrain limbic circuits in both an experience-independent and experiencedependent manner.…”

Section: Discussionsupporting

confidence: 85%

Experience-dependent resonance in amygdalo-cortical circuits supports fear memory retrieval following extinction

Ozawa

Davis

et al. 2020

Nat Commun

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Learned fear and safety are associated with distinct oscillatory states in the basolateral amygdala (BLA) and medial prefrontal cortex (mPFC). To determine if and how these network states support the retrieval of competing memories, we mimicked endogenous oscillatory activity through optogenetic stimulation of parvalbumin-expressing interneurons in mice during retrieval of contextual fear and extinction memories. We found that exogenously induced 4 Hz and 8 Hz oscillatory activity in the BLA exerts bi-directional control over conditioned freezing behavior in an experience-and context-specific manner, and that these oscillations have an experience-dependent ability to recruit distinct functional neuronal ensembles. At the network level we demonstrate, via simultaneous manipulation of BLA and mPFC, that experience-dependent 4 Hz resonance across BLA-mPFC circuitry supports postextinction fear memory retrieval. Our findings reveal that post-extinction fear memory retrieval is supported by local and interregional experience-dependent resonance, and suggest novel approaches for interrogation and therapeutic manipulation of acquired fear circuitry.

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Section: Discussionsupporting

confidence: 85%

Experience-dependent resonance in amygdalo-cortical circuits supports fear memory retrieval following extinction

Ozawa

Davis

et al. 2020

Nat Commun

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“…In the present study, it was not possible to analyze the temporal pattern of activity in the 3-5 Hz delta band due to edge effects due to shock artefact. However, others have found that a 4Hz oscillation develops in the mPFC during freezing behavior and that this oscillation was driven by respiration (Moberly et al, 2016;Karalis et al, 2016;Bagur and Benchenane, 2018). In line with these studies, we recently showed that respiratory frequency and delta activity frequency were highly correlated during freezing (Dupin et al, 2019).…”

Section: Does Respiratory Rhythm Modulate the Temporal Patterns Obsersupporting

confidence: 85%

Respiration and brain neural dynamics associated with interval timing during odor fear learning in rats

Dupin¹,

Garcia²,

Messaoudi³

et al. 2020

Preprint

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In fear conditioning, where a conditioned stimulus predicts the arrival of an aversive stimulus, the animal encodes the time interval between the two stimuli. Freezing, the most used index to assess learned fear, lacks the temporal resolution required to investigate interval timing at the early stages of learning. Here we monitored respiration to visualize anticipatory behavioral responses in an odor fear conditioning in rats, while recording theta (5-15Hz) and gamma (40-80Hz) brain oscillatory activities in the medial prefrontal cortex (mPFC), basolateral amygdala (BLA), dorsomedial striatum (DMS) and olfactory piriform cortex (PIR). We investigated the temporal patterns of respiration frequency and of theta and gamma activity power during the odor-shock interval. We found that akin to respiration patterns, theta temporal curves were modulated by the duration of the odor-shock interval in the four recording sites, and respected scalar property in mPFC and DMS. In contrast, gamma temporal curves were modulated by the interval duration only in the mPFC, and in a manner that did not respect scalar property. This suggests a preferential role for theta rhythm in interval timing. In addition, our data bring the novel idea that the respiratory rhythm might take part in the setting of theta activity dynamics.

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“…In the present study, it was not possible to analyze the temporal pattern of activity in the 3–5 Hz delta band due to edge effects surrounding the shock artefact. However, others have found that a 4 Hz oscillation develops in the mPFC during freezing behavior and that this oscillation was driven by respiration 43 – 45 . In line with these studies, we recently showed that respiratory frequency and delta activity frequency were highly correlated during freezing 29 .…”

Section: Discussionmentioning

confidence: 97%

Respiration and brain neural dynamics associated with interval timing during odor fear learning in rats

Dupin

Garcia

Messaoudi

et al. 2020

Sci Rep

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In fear conditioning, where a conditioned stimulus predicts the arrival of an aversive stimulus, the animal encodes the time interval between the two stimuli. Here we monitored respiration to visualize anticipatory behavioral responses in an odor fear conditioning in rats, while recording theta (5–15 Hz) and gamma (40–80 Hz) brain oscillatory activities in the medial prefrontal cortex (mPFC), basolateral amygdala (BLA), dorsomedial striatum (DMS) and olfactory piriform cortex (PIR). We investigated the temporal patterns of respiration frequency and of theta and gamma activity power during the odor-shock interval, comparing two interval durations. We found that akin to respiration patterns, theta temporal curves were modulated by the duration of the odor-shock interval in the four recording sites, and respected scalar property in mPFC and DMS. In contrast, gamma temporal curves were modulated by the interval duration only in the mPFC, and in a manner that did not respect scalar property. This suggests a preferential role for theta rhythm in interval timing. In addition, our data bring the novel idea that the respiratory rhythm might take part in the setting of theta activity dynamics related to timing.

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Dissociation of fear initiation and maintenance by breathing-driven prefrontal oscillations

Cited by 11 publications

References 46 publications

Experience-dependent resonance in amygdalo-cortical circuits supports fear memory retrieval following extinction

Experience-dependent resonance in amygdalo-cortical circuits supports fear memory retrieval following extinction

Respiration and brain neural dynamics associated with interval timing during odor fear learning in rats

Respiration and brain neural dynamics associated with interval timing during odor fear learning in rats

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