Oxytocin, Neural Plasticity, and Social Behavior

Abstract

Oxytocin regulates parturition, lactation, parental nurturing, and many other social behaviors in both sexes. The circuit mechanisms by which oxytocin modulates social behavior are receiving increasing attention. Here, we review recent studies on oxytocin modulation of neural circuit function and social behavior, largely enabled by new methods of monitoring and manipulating oxytocin or oxytocin receptor neurons in vivo. These studies indicate that oxytocin can enhance the salience of social stimuli and increase signal-to-noise ratios by modulating spiking and synaptic plasticity in the context of circuits and networks. We highlight oxytocin effects on social behavior in nontraditional organisms such as prairie voles and discuss opportunities to enhance the utility of these organisms for studying circuit-level modulation of social behaviors. We then discuss recent insights into oxytocin neuron activity during social interactions. We conclude by discussing some of the major questions and opportunities in the field ahead. Expected final online publication date for the Annual Review of Neuroscience, Volume 44 is July 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

“…This facilitates the release of more glutamate upon activation of the pre-synaptic neurons (Figure 1E,F and 2E,F), while leaving spontaneous synaptic transmission unchanged (Figure 1B and C). Such an OXT-dependent mechanism could help filter salient inputs to the NAc – similar to how OXT enhances the signal-to-noise ratio in other brain areas (Owen et al 2013; Oettl et al 2016; Froemke and Young 2021) by a mechanism that here involves the modulation of another neuromodulatory system: the eCB system. Furthermore, we hereby demonstrate that such an OXT-dependent modulation of glutamatergic transmission can depend on the context defined by the socio-sexual experience.…”

“…Oxytocin (OXT) is a key neuromodulator for the regulation of social behaviors (Froemke and Young 2021; Johnson and Young 2017), and a target for the treatment of neuropsychiatric disorders (Meyer-Lindenberg et al 2011; DeMayo et al 2019; Ford and Young 2021). OXT is produced mainly by neurons located in the supra-optic and paraventricular nuclei of the hypothalamus.…”

Oxytocin facilitates communicative adjustments by upregulating broadband aperiodic activity in the prefrontal cortex

“…Given the presence of oxytocin receptors in the post-orbital gyrus in human brain (Boccia et al, 2013), it is possible that oxytocin regulates recipient design via a direct impact on vPFC neural activity. However, oxytocin effects are also mediated through other neurotransmitter systems, such as the dopaminergic and the serotoninergic systems, influencing several prefrontal-amygdala circuits (Froemke & Young, 2021;Gangopadhyay et al, 2021;Love, 2014;Ma et al, 2016;Martins et al, 2021;Quintana et al, 2019;Sripada et al, 2013;Striepens et al, 2014). Future studies might differentiate these potential mechanisms with high-precision M/EEG (Seeber et al, 2019;Tzovara et al, 2019) and newly developed algorithms for source reconstruction (Krishnaswamy et al, 2017;Pizzo et al, 2019) that are able to disentangle activities from deeper limbic structures.…”

Mate Choice, Sex Roles and Sexual Cognition: Neuronal Prerequisites Supporting Cognitive Mate Choice

“…Many of these pathways are thought to be evolutionary conserved and operate similarly in many vertebrate taxa. Various neurotransmitters (e.g., dopamine and serotonin), opioid peptides, (sex) steroid hormones (e.g., testosterone and estrogens), corticosteroids, neurosteroids, and neuropeptides (e.g., oxytocin or argininevasopressin) precisely modulate the interplay of different neuronal networks, including the mesolimbic reward system, the SBN, the social salience network and other brain regions involved in social and/or sexual recognition as well as learning in the contexts of mate choice (Choleris et al, 2009(Choleris et al, , 2012O'Connell and Hofmann, 2011;Gabor et al, 2012;Goodson, 2013;Petrulis, 2013;Ervin et al, 2015;Dumais and Veenema, 2016;Ashley and Demas, 2017; but see Kavaliers and Choleris, 2017;Froemke and Young, 2021 for review). For instance, in adult and larval zebrafish, the neuro-endocrine system, namely the fish ortholog of oxytocin (i.e., isotocin or 'zebrafish oxytocin') and, possibly, the fish ortholog of mammalian vasopressin (i.e., vasotocin or 'zebrafish vasopressin') appeared to support their social behavior and social preference, but not anxiety-related behavior (Landin et al, 2020).…”