Vasopressin modulates social recognition-related activity in the left temporoparietal junction in humans

Abstract

The neuropeptide vasopressin is a key molecular mediator of social behavior in animals and humans, implicated in anxiety and autism. Social recognition, the ability to assess the familiarity of others, is essential for appropriate social interactions and enhanced by vasopressin; however, the neural mechanisms mediating this effect in humans are unknown. Using functional magnetic resonance imaging (fMRI) and an implicit social recognition matching task, we employed a double-blinded procedure in which 20 healthy male volunteers self-administered 40 UI of vasopressin or placebo intranasally, 45 min before performing the matching task in the scanner. In a random-effects fMRI analysis, we show that vasopressin induces a regionally specific alteration in a key node of the theory of mind network, the left temporoparietal junction, identifying a neurobiological mechanism for prosocial neuropeptide effects in humans that suggests novel treatment strategies.

Human neuroimaging of oxytocin and vasopressin in social cognition

“…To date, pharmacological fMRI studies investigating the effects of vasopressin on neural activity related to social cognition are far outnumbered by those of oxytocin; yet a few studies, using double-blind, placebo-controlled procedures, have demonstrated distinct neural activation patterns related to intranasal administration of vasopressin in men (Rilling et al, 2011; Zink et al, 2011; Zink et al, 2010). Despite the marked structural similarity between vasopressin and oxytocin – differing in only two amino acids – administration of vasopressin modulates activity in discrete brain regions, and perhaps particularly striking is a lack of direct vasopressin influence on amygdala reactivity, at least at this time.…”

“…In rodents, the lateral septum, a brain region connected to the olfactory system, has been critically implicated in the actions of vasopressin to influence social recognition (Bielsky et al, 2005), but given that humans rely primarily on auditory and visual information for social recognition, cortical areas with access to multimodal auditory/visual information are perhaps more likely to underlie the influence of vasopressin on social familiarity in humans. In a vasopressin pharmacological fMRI study designed to investigate precisely that, Zink et al (2011) employed a matching paradigm that again, similar to the previous study (Zink et al, 2010), entailed implicit processing of emotional stimuli, but now with an added component related to stimuli familiarity. Male participants matched familiar (previous exposure) and unfamiliar (first exposure) faces expressing negative affect or negative scene orientations as a non-social control condition.…”

“…A 40 IU administration of vasopressin modulated social recognition-related left TPJ activity – a brain region highly implicated in social cognitive processes (Van Overwalle, 2009), including the processing of social background context and familiarity (Gobbini and Haxby, 2007; Saxe and Wexler, 2005) – as assessed with the interaction of sociality and familiarity of presented stimuli. Specifically, during exposure to socially unfamiliar stimuli, vasopressin abolished the left TPJ activation evoked by social unfamiliarity under placebo to a level comparable to that elicited by social familiar stimuli under placebo (Zink et al, 2011). These findings suggest that under vasopressin, stimuli are more readily transferred to a familiar categorization, as represented in TPJ reactivity.…”

The Effects of Acute Arginine Vasopressin Administration on Social Cognition in Healthy Males

“…Thompson and colleagues showed that AVP enhances facial responses to neutral facial stimuli in men [9] as well as demonstrating sexually dimorphic effects in men and women on affiliative and aggressive facial motor responses to unfamiliar faces of the same sex [10]. Of particular note, neural evidence suggests that intranasal AVP administration alters activity in the temporoparietal junction when processing social information, a key area for theory of mind tasks [11], and potentially alters medial prefrontal cortex connectivity to the amygdala during exposure to emotionally negative faces [12]. Taken together, these findings suggest that intranasal AVP may modulate social cognitive functioning at both behavioral and neural levels.…”

Common polymorphism in the oxytocin receptor gene ( OXTR ) is associated with human social recognition skills

“…In rodents, as well as many other species, the primary cues used in this recognition process are olfactory or pheromonal, but in primates visual and auditory processes are of paramount importance. Evidence is building that the neuropeptides oxytocin and arginine-vasopressin are critically involved in the development of social recognition in rodent species (3)(4)(5)(6), primates (7), and humans (8)(9)(10)(11).…”