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Journal Articles Scientific Reports Year : 2020

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


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. Interval timing refers to the ability to time intervals ranging from seconds to minutes and guides fundamental animal behaviors like the anticipation of rewarding or aversive events. The tasks classically used in the literature to assess interval timing in animals, necessitate numerous training sessions and involve a motor response from the animal 1. Yet some studies show that in associative learning, animals learn to time the arrival of reinforcement from the outset of conditioning 2-7 and such temporal encoding has been suggested to be a fundamental component of associative learning 8. However, the neurobiological basis of interval timing in Pavlovian associative learning remain poorly understood, due in part to the paucity of studies designed for its investigation 9. In a previous study using odor fear conditioning in rats, we showed that, when using an appropriate index, namely the respiratory rate, interval timing can be inferred from the animal's behavior after a few training trials 7. More specifically, the animal's respiratory rate was monitored in this paradigm where an initially neutral odor signals the arrival of an aversive mild foot-shock at a fixed time interval. We showed that after a few odor-shock pairings, the respiratory frequency curve presented a temporal pattern that was linked to the duration of the interval to be timed, in a manner that respected scalar property, a hallmark of interval timing, i.e. the error magnitude in estimating a duration was proportional to the duration to be timed 10. Based on these findings, in the present study we investigated the neural network dynamics occurring during the odor-shock interval in odor fear conditioning in rats. Although the neural mechanisms underlying timing remain largely unknown, several studies in the literature reported dynamically changing patterns of activity that contain information about elapsed time since a given stimulus. This property has been found in multiple brain areas including the dorsal striatum and the prefrontal cortex 11,12. More specifically, electrophysiological recording of neurons in the medial prefrontal cortex (mPFC) and the dorsomedial striatum (DMS) in rats engaged in interval timing, have shown that ramping activity, a monotonic change in neuronal firing rate across time, is observed throughout frontostriatal ensembles. Importantly, DMS ramping neurons were shown to synchronize with mPFC 4-Hz activity and inactivation of the mPFC impaired interval timing and attenuated ramping OPEN
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hal-02992673 , version 1 (06-11-2020)





Maryne Dupin, Samuel Garcia, Belkacem Messaoudi, Valérie Doyère, Anne-Marie M Mouly. Respiration and brain neural dynamics associated with interval timing during odor fear learning in rats. Scientific Reports, 2020, 10 (1), pp.17643. ⟨10.1038/s41598-020-74741-2⟩. ⟨hal-02992673⟩
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