The Role and Properties of Neurons in the Medial Preoptic Area in Paternal Care of California Mice (Peromyscus californicus)

The neurobiological basis of and factors facilitating male parental behavior are not well understood in mammals. Multiple rodent species show increases in parental behavior during the transition into parenthood or after prolonged exposure to pups. For the first time, we evaluated effects of prior exposure to pups on paternal responsiveness in the biparental California mouse (Peromyscus californicus). Adult virgin male California mice exhibit aggressive or indifferent responses to pups more frequently than fathers, which exhibit robust paternal care. We analyzed behavioral, neural, and corticosterone responses to pups in adult virgin males that were interacting with a pup for the first time, adult virgin males that had been exposed to pups 3 times for 20 min each in the previous week, and first-time fathers. Control groups of virgins were similarly tested with a novel object (i.e., a marble). Previous exposure to pups increased paternal care: responses to pups did not differ between virgins with repeated exposure to pups and new fathers. Neither basal corticosterone levels nor corticosterone levels following acute pup or marble exposure differed among groups. Finally, Fos expression in the medial preoptic area (MPOA) and bed nucleus of the stria terminalis was higher following exposure to a pup than to a marble. Fos expression was not, however, affected by previous exposure to these stimuli. These results suggest that previous experience with pups can increase paternal responsiveness via unknown mechanisms. To investigate these mechanisms, we evaluated synaptic, intrinsic, and morphological properties of MPOA neurons in male virgins or first-time fathers using standard whole-cell recordings in a novel in vitro slice preparation. We measured synaptic currents in response to local electrical stimulation, and we quantified intrinsic excitability by measuring voltage changes in response to square-pulse injections of both depolarizing and hyperpolarizing current. We also analyzed the morphology of MPOA neurons. Most parameters did not differ significantly between virgins and fathers. However, we documented a decrease in synaptic inhibition in fathers. These findings suggest that the onset of paternal behavior in California mouse fathers may be associated with limited electrophysiological plasticity within the MPOA