Neural control of maternal and paternal behaviors

Abstract

Parental care, including feeding and protection of young, is essential for the survival as well as mental and physical well-being of the offspring. A large variety of parental behaviors has been described across species and sexes, raising fascinating questions about how animals identify the young and how brain circuits drive and modulate parental displays in males and females. Recent studies have begun to uncover a striking antagonistic interplay between brain systems underlying parental care and infant-directed aggression in both males and females, as well as a large range of intrinsic and environmentally driven neural modulation and plasticity. Improved understanding of the neural control of parental interactions in animals should provide novel insights into the complex issue of human parental care in both health and disease.

Fig. 1. Paternal care can be observed in many different taxa

(A) Giant water bug (Abedus herberti). (B) Los Tayos rocket frog (Hyloxalus nexipus). (C) Silverback mountain gorilla (Gorilla beringei beringei) father with infants. [Photos by Ivan Phillipsen (A), Adam Stuckert (B), Lubert Stryer (C)]

Fig. 2. Evolution of diverse and distinct parental cares strategies across the animal kingdom

Examples of different parental care strategies are shown across vertebrates and invertebrates. Male uniparental care is lacking only in the mammalian and reptilian lineages, although there are male-biased parental care systems in few canids and primates. (A) Common deer mouse (Peromyscus maniculatus). (B) Oldfield mouse (Peromyscus polionotus). (C) Kori bustard (Ardeotis kori). (D) Adélie penguin (Pygoscelis adeliae). (E) Pheasant-tailed jacana (Hydrophasianus chirurgus). (F) Water python (Liasis fuscus). (G) Black rock skink (Egernia saxatilis). (H) Diablito frog (Oophaga sylvatica). (I) Mimic poison frog (Ranitomeya imitator). (J) Dyeing poison frog (Dendrobates tinctorius). (K) Burton’s mouthbrooder (Astatotilapia burtoni). (L) Convict cichlid (Amatitlania nigrofasciata). (M) Three-spined stickleback (Gasterosteus aculeatus). (N) Golden brown stink bug (Anchises parvulus). (O) Burying beetle (Nicrophorus vespilloides). (P) Giant water bug (Abedus herberti). [Photos by Andrés Bendesky (A and B), Tamas Szekely (C), Oliver Kruger (D), Ghulam Rasool (E), Zachary Stahlschmidt (F), Alan Couch (G), Elicio E. Tapia (H), Evan Twomey (I), Lauren A. O’Connell (J), Rayna Harris (K), Bryan J. Matthews (L), Dwight Kuhn (M), Peter Chew at www.brisbaneinsects.com (N), Allen Moore (O), Michael Bogan (P)]

Fig. 3. Pup-directed behavior of males at different days after mating [replotted from (50), table 2]

Adult male mice of the CF-1 strain were mated with females, randomly assigned into groups, and tested at different days after mating. Control virgin males are plotted at day 0. After a significant increase in pup-directed aggression at day 4, there is a transient suppression of attack and increase in paternal care in the males from day 12 to day 50, which approximately corresponds to the birth of and the weaning of their own pups. This experiment illustrates a remarkable influence of mating on male parental behavior.

Fig. 4. Schematic presentation of brain areas associated with parental care (A) and pup-directed avoidance and aggression (B)

Solid lines denote projections that are involved in the regulation of pup-directed behavior, as supported by direct evidence. Dashed lines denote known connections that exist between these areas and are potentially involved in the behavior. The lines and arrows simply denote origins and targets and do not represent actual axon path or excitatory inputs. Not all the known connections are shown. Abbreviations of brain areas: MOB, main olfactory bulb; PFC, prefrontal cortex; NAc, nucleus accumbens; VP, ventral pallidum; LSd, lateral septum, dorsal part; LSi, lateral septum, intermediate part; vBNST, bed nucleus of stria terminalis, ventral part; MPOA, medial preoptic area; PVNm, paraventricular nucleus, magnocellular part; BL, basolateral amygdala; Ce, central amygdala; VTA, ventral tegmental area; PAG, periaqueductal gray; Raphe, Raphe nucleus; LC, locus coeruleus; AOB, accessory olfactory bulb; LSv, lateral septum, ventral part; BNSTpr, bed nucleus of stria terminalis, principal nucleus; PVNp, paraventricular nucleus, parvocellular part; DMH, dorsomedial hypothalamic nucleus; VMH ventromedial hypothalamic nucleus; MeA, medial amygdala; PMd, premammillary nucleus, dorsal part.

Fig. 5. MPOA Gal neurons serve as an essential regulatory node for parental care in both male and female mice

(A) Co-labeling of c-fos and Gal in the MPOA of parenting females. (B) Cumulative percentages of virgin females that retrieved or attacked pups as a function of the percentage of remaining Gal cells after Gal cell ablation. Reference cell number (100%) is the average MPOA Gal cell number in the control group. (C) Cumulative percentages of fathers that retrieved pups as a function of remaining Gal cells after Gal cell ablation. (D) Behavior raster plots after optogenetic activation of Gal cells in virgin males interacting with pups. The control group consisted of littermates that do not express light-activated channelrhodopsin-2. Different behavior elements are color-coded and could occur simultaneously.