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Somatosensory stimuli trigger coordinated oxytocin neurons activity during social interaction

Benusiglio, Diego

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Abstract

The hypothalamic neuropeptide oxytocin (OT) promotes social communication via its central release in the mammalian brain. However, how social interaction affects electrical activity of OT neurons is still unclear. To address this question, I used cell-type specific viral vectors in combination with optoelectrode-based techniques. I performed the in vivo single-unit recording of optically identified OT neurons in the paraventricular nucleus (PVN) of hypothalamus in adult female rats during their social interactions with unfamiliar female conspecifics. Simultaneously, we monitored behavior and recorded ultrasonic vocalizations. The results showed that active social interactions events induce an increase of PVN OT neurons spiking activity as well as a re-organization of the firing pattern from regular to bursting. The action potentials of simultaneously recorded OT neurons were synchronized and phase-locked with the PVN theta oscillations precisely at the time of social interactions, but not during non-social exploratory behavior. To decipher which sensory stimuli trigger OT neuron activity, I performed experiments with partial deprivation of specific sensory modalities. Direct physical contact between rats, or even gentle skin stimulation, led to a profound increase in OT firing rates. In contrast, presentation of visual, auditory and olfactory social-relevant stimuli alone did not significantly alter OT neuron activity. This led to the conclusion somatosensory component of social interaction drives OT neurons synchronous activity. To further explore the effects of tactile stimuli on the OT system, I examined the expression of the marker of neuronal activity c-Fos after repetitive somatosensory stimulation; it appeared to be significantly increased in a particular subpopulation of OT neurons named parvocellular OT neurons. Employing in-vivo calcium recording via fiber photometry, I investigated the role of parvocellular OT neurons in regulating the activity of the general population of PVN OT neurons, finding that parvocellular OT neurons mediate the activation of the OT system in response to somatosensory stimuli. Next, I selectively modulated the activity of parvocellular OT neurons in awake freely moving rats via pharmacogenetics: activation of this population of neurons resulted in increased social interaction, while inhibition leaded to decrease of social interaction. Finally, I studied the effect of intracerebral infusion of an OT receptor antagonist which induced a substantial reduction of social interaction time, even when parvocellular OT neurons were activated. Altogether, these results indicate that somatosensory stimulation is essential to activate OT neuron ensembles and, hence, can induce central neuropeptide release in socially interacting female rats. This opens perspectives for studying functional and anatomical connectivity between the somatosensory and OT systems in normal and psychopathological conditions.

Item Type: Dissertation
Supervisor: Grinevich, Prof. Dr. Valery
Date of thesis defense: 10 September 2019
Date Deposited: 18 Sep 2019 09:33
Date: 2020
Faculties / Institutes: The Faculty of Bio Sciences > Dean's Office of the Faculty of Bio Sciences
Subjects: 500 Natural sciences and mathematics
Controlled Keywords: Oxytocin, Social interaction
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