A calcitonin receptor-expressing subregion of the medial preoptic area is involved in alloparental tolerance in common marmosets

Abstract

Like humans, common marmoset monkeys utilize family cooperation for infant care, but the neural mechanisms underlying primate parental behaviors remain largely unknown. We investigated infant care behaviors of captive marmosets in family settings and caregiver-infant dyadic situations. Marmoset caregivers exhibited individual variations in parenting styles, comprised of sensitivity and tolerance toward infants, consistently across infants, social contexts and multiple births. Seeking the neural basis of these parenting styles, we demonstrated that the calcitonin receptor-expressing neurons in the marmoset medial preoptic area (MPOA) were transcriptionally activated during infant care, as in laboratory mice. Further, site-specific neurotoxic lesions of this MPOA subregion, termed the cMPOA, significantly reduced alloparental tolerance and total infant carrying, while sparing general health and other social or nonsocial behaviors. These results suggest that the molecularly-defined neural site cMPOA is responsible for mammalian parenting, thus provide an invaluable model to study the neural basis of parenting styles in primates.

Anxious about rejection, avoidant of neglect: Infant marmosets tune their attachment based on individual caregiver’s parenting style

“…Infant carrying impedes the carrier’s locomotor activities and thus is shared by the family members: the mother, father, and older siblings 36 . Our previous study 37 identified two independent (allo)parenting parameters, sensitivity to infant distress and tolerance to infant carrying, similar to parenting styles established in humans 38 , 39 . Furthermore, the molecularly defined subregion of the medial preoptic area in the basal forebrain specifically regulates caregivers’ tolerance in marmosets 37 .…”

Parental brain through time: The origin and development of the neural circuit of mammalian parenting

“…We, therefore, examined the MPOA of common marmosets, a New World monkey species that utilizes family cooperation with vocal communication for infant care like humans. We found a CALCR + neuron cluster in a small subregion of the marmoset posterior MPOA that colocalized with c‐Fos after alloparental care 87 . Voxel‐based, lesion–behavior mapping identified that the CALCR + MPOA subregion is responsible for infant‐carrying tolerance (the ability to endure infant carrying without physically rejecting the infants) without affecting general health, locomotion, and other social behaviors with family members.…”

“…We found a CALCR + neuron cluster in a small subregion of the marmoset posterior MPOA that colocalized with c-Fos after alloparental care. 87 Voxelbased, lesion-behavior mapping identified that the CALCR + MPOA subregion is responsible for infant-carrying tolerance (the ability to endure infant carrying without physically rejecting the infants) without affecting general health, locomotion, and other social behaviors with family members. Furthermore, amylin administration to the marmoset cMPOA facilitated infant carrying, 139 plausibly by binding and activating CALCR + neurons, which has also been shown in mice.…”

“…Thus, to demonstrate the specificity of the behavioral alteration, 114,115 the lesion experiments should be accompanied by appropriate control experiments, such as similar-sized lesions of another brain area and the inclusion of nontargeted behavioral assessments, such as general physiological fitness and locomotion. 76,78,87,116 Also, associated null results (i.e., the lesion did not affect another behavior) are very informative to show the selectivity of the target brain region for a given behavior. For example, MPOA lesions in rats and mice that dis-rupt maternal care do not grossly affect female sexual behaviors or parturition of average numbers of litters.…”

“…Michael Numan presented a seminal series of studies demonstrating that the MPOA (Figure 1) is responsible for rat maternal care, possibly through its dorsolateral connections with the brain stem, such as the ventral tegmental area (VTA). [76][77][78][79][80] Since then, the MPOA has been established as the brain hub for maternal, paternal, and alloparental nurturing behaviors, with evidence in laboratory rats, 76,81,82 hamsters, 83 biparental California mice, 84 laboratory mice, 55 rabbits, 85 sheep, 86 common marmoset monkeys (Callithrix jacchus), 87 and with supporting observations in humans 88,89 29,30 Still, there are practical benefits of the classical practice that deals with them together as a continuum (Figure 1A). 31 First, the POA and hypothalamus are spatially adjacent and extensively connected through the longitudinal fiber system.…”