Figure 4.

Hypothesis in which development shines light on the ‘Dark Matter of Social Neuroscience’, or the unclarified neural mechanisms between social sensory inputs and social behavior outputs (Insel, 2010). (a) During developmental sensitive periods, parental nurturing (Kojima et al, 2012; Weisman et al, 2012) and/or sensory inputs (Zheng et al, 2014) drive the activity of the PVN resulting in increased release of oxytocin. This oxytocin can regulate multi-sensory plasticity in the neocortex. (b) OXTRs are transiently available during experience-dependent developmental sensitive periods (Hammock and Levitt, 2013). Arrows point to layer II/III of neocortex, which has a high density at postnatal day 14, but not postnatal day 21 or later ages. Perhaps this entrains the developing brain to attend to relevant stimuli, which acquire social definitions because of their proximity in time and space to the nurturing caregiver. After such a developmental trajectory, an adult brain is tuned to ascribe social, affect-modulating properties to multisensory information. (c) For example, wild-type mice are tuned to social stimuli and can rapidly resolve sensory input to determine if a mouse is familiar or novel. In contrast, oxytocin knock-out mice are unable to resolve this social sensory information, despite very active neural processing in primary sensory cortex as measured by c-Fos immunoreactivity after a social encounter (Ferguson et al, 2001), c-Fos images courtesy of Dr Larry Young, copyright The Society for Neuroscience; hatched box at P21 in ‘b’ indicates cortical barrel fields measured in young adult (>P50) mice in panel (c). Thus, developmentally transient experience-dependent neocortical oxytocin signals may allow social support (ie, maternal contact) to fine tune the function of the entire neocortex during a developmental sensitive period for social contact. This layer II/III positioning makes OXTR a promising modulator of multi-sensory integration across modalities by changing the window of opportunity in which separate neural signals could be bound into one unified percept. Developmental modulation in this way by other classic neuroendocrine modulators (eg, CRF, vasopressin) during various sensitive periods may have a significant role in the species-typical development of the brain.