Oxytocin enables maternal behaviour by balancing cortical inhibition

Abstract

Oxytocin is important for social interactions and maternal behavior. However, little is known about when, where, and how oxytocin modulates neural circuits to improve social cognition. Here we show how oxytocin enables pup retrieval behavior in female mice by enhancing auditory cortical pup call responses. Retrieval behavior required left but not right auditory cortex, was accelerated by oxytocin in left auditory cortex, and oxytocin receptors were preferentially expressed in left auditory cortex. Neural responses to pup calls were lateralized, with co-tuned and temporally-precise excitatory and inhibitory responses in left cortex of maternal but not pup-naive adults. Finally, pairing calls with oxytocin enhanced responses by balancing the magnitude and timing of inhibition with excitation. Our results describe fundamental synaptic mechanisms by which oxytocin increases the salience of acoustic social stimuli. Furthermore, oxytocin-induced plasticity provides a biological basis for lateralization of auditory cortical processing.

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

“…Indeed, OT has been shown to increase spike output [89][90][91] and facilitate synaptic long-term potentiation [92][93][94] and our data suggest an intrinsic mechanism that may underlie shifts in synaptic efficacy and excitatory/inhibitory balance found in brain regions where OT is critical for myriad social behaviors 67,74,90,95 . Intrinsic properties are shaped by ion channels.…”

“…Given the dense expression of OTR in the insula and evidence that OT can modulate excitatory balance in cortical circuits 67 , we hypothesized that OT released during the SAP test could directly modulate insular cortex excitability. The excitability of insular cortex was characterized after bath application of OT (500nM) in whole-cell pyramidal neuron recordings ( Fig.…”

C-tactile afferents: Cutaneous mediators of oxytocin release during affiliative tactile interactions?

“…It has previously been shown that female mice with maternal experience display higher signal to noise ratios in their neural responses to pup cries than virgin females within this region (Liu et al, 2006;Rothschild et al, 2013). Marlin et al (2015) demonstrated that when housed with an experienced dam and her pups, virgin female mice receiving either systemic injections of oxytocin or optogenetic stimulation within the PVN started retrieving pups significantly earlier than saline treated virgins who required at least 2 days of co-housing before they expressed retrieval behaviour. In fact, systemic or central release of oxytocin triggered retrieval in virgin dams even without cohousing.…”

“…A recent study by Marlin et al (2015) demonstrated that the acquisition of pup retrieval behaviour by female mice is dependent on the modulatory actions of oxytocin within auditory cortex. It has previously been shown that female mice with maternal experience display higher signal to noise ratios in their neural responses to pup cries than virgin females within this region (Liu et al, 2006;Rothschild et al, 2013).…”

Neuroscience: The hard science of oxytocin

“…Then, as the oxytocin kicked in, the signal evolved into a more orderly pattern typical of a maternal brain. The study showed in unusual detail how the hormone changed the behaviour of neurons 1 . "Oxytocin is helping to transform the brain, to make it respond to those pup calls, " Froemke says.…”