Forebrain peptides modulate sexually polymorphic vocal circuitry

Abstract

The peptide arginine-vasopressin (mammals) and its evolutionary precursor arginine-vasotocin (non-mammals) modulate reproductive physiology and numerous related social behaviours, as do oxytocin (mammals) and its homologues mesotocin and isotocin (fish). The distributions in the brain and/or the behavioural functions of these peptides often differ between the sexes, and between species with divergent social structures. Here we present neurophysiological evidence that males with vocal characteristics typical of females share a pattern of neuropeptide function with females rather than conspecific males. The plainfin midshipman fish (Porichthys notatus) has two male morphs with different reproductive tactics and vocalizations (a key species-typical behaviour which varies in its physical attributes and contextual usage, depending on the morph's social strategy). Forebrain-evoked, rhythmic vocal-motor activity that precisely mimics natural vocalizations was modulated by arginine-vasotocin, isotocin and their antagonists delivered to the preoptic area-anterior hypothalamus, a primary site for behavioural integration in all vertebrates. Peptides had different effects in males that acoustically court females (arginine-vasotocin-sensitive) than in females and sneak-spawning males (isotocin-sensitive), showing that the neuromodulatory mechanisms that establish reproduction-related behaviour can be dissociated from gonadal sex.