Social Bonding and the Brain: Oxytocin’s role in a neural circuit for maternal social behavior

Oxytocin is a neuropeptide important for controlling social behaviors such as pair bonding and parenting. It does this in part by increasing the salience of socially relevant sensory input. However, it has not been clear which neurons in the brain respond to oxytocin, or how oxytocin modifies neural circuits to increase the prominence of social information.  A recent study by Marlin et al. examined the role of oxytocin in social behavior, using a mouse model to investigate a common mammalian maternal behavior, pup retrieval.

When separated from their mothers, mouse pups emit ultrasonic distress calls that mothers use to locate and retrieve their pups. Naïve females generally do not retrieve pups, but can learn to recognize the distress calls and will begin to retrieve pups when housed with mothers and their pups. The authors sought to understand how oxytocin was important in neural plasticity in the auditory cortex—the brain region important for hearing the pups’ distress calls—by training naïve females to retrieve pups in order to examine changes in the brain.

The investigators found neurons responding to oxytocin were lateralized to the left auditory cortex in the experienced females. Inactivation of the left auditory cortex impaired pup retrieval, but inactivation of the right auditory cortex had no such effect. The authors recorded the activity of individual neurons in the left auditory cortex in vivo, and found that pups calls (but not pure tones) evoked stronger responses in neurons from experienced females compared to naïve females. Marlin and colleagues also examined synaptic responses by voltage-clamp recording synaptic currents in the auditory cortex, and found that excitation and inhibition were tuned and precisely timed in the left auditory cortex of experienced females. This balance was not found in the right auditory cortex or in the left auditory cortex of naïve females.

Marlin and colleagues then tested whether oxytocin modified neural circuit activity. Stimulation of oxytocin-responding neurons in the auditory cortex of experienced females resulted in reduced inhibitory post-synaptic currents and a gradual increase in excitatory post-synaptic currents, which led to disinhibition of the auditory cortex. Significantly, when the investigators paired pup calls with stimulation of oxytocin-responding neurons or administration of oxytocin in the left auditory cortex in naïve females, they observed the same disinhibition of neurons found in experienced females. These results indicate that oxytocin modulates neuronal activity in the left auditory cortex in response to pup distress cries.

These findings suggest that there is functional lateralization in the auditory cortex, a phenomenon also found in human speech processing in the temporal lobe. Together, these data illustrate that oxytocin in a specific neuronal circuit is important for a complex maternal social behavior.

Publication

1. Marlin BJ, Mitre M, D’amour JA, Chao MV, Froemke RC (2015) Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520:499-504. doi: 10.1038/nature14402