skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Early life social complexity shapes adult neural processing in the communal spiny mouse Acomys cahirinus
Rationale Early life social rearing has profound consequences on offspring behavior and resilience. Yet, most studies examining early life development in rodents use species whose young are born immobile and do not produce complex social behavior until later in development. Furthermore, models of rearing under increased social complexity, rather than deprivation, are needed to provide alternative insight into the development of social neural circuitry. Objectives To understand precocial offspring social development, we manipulated early life social complexity in the communal spiny mouse Acomys cahirinus and assessed long-term consequences on offspring social behavior, exploration, and neural responses to novel social stimuli. Methods Spiny mouse pups were raised in the presence or absence of a non-kin breeding group. Upon adulthood, subjects underwent social interaction tests, an open field test, and a novel object test. Subjects were then exposed to a novel conspecific and novel group and neural responses were quantified via immunohistochemical staining in brain regions associated with social behavior. Results Early life social experience did not influence behavior in the test battery, but it did influence social processing. In animals exposed to non-kin during development, adult lateral septal neural responses toward a novel conspecific were weaker and hypothalamic neural responses toward a mixed-sex group were stronger. Conclusions Communal species may exhibit robust behavioral resilience to the early life social environment. But the early life environment can affect how novel social information is processed in the brain during adulthood, with long-term consequences that are likely to shape their behavioral trajectory.  more » « less
Award ID(s):
2011001 2310626
PAR ID:
10501873
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Psychpharmacology
Date Published:
Journal Name:
Psychopharmacology
ISSN:
0033-3158
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract In complex social environments, individuals may interact with not only novel and familiar conspecifics but also kin and non-kin. The ability to distinguish between conspecific identities is crucial for most animals, yet how the brain processes conspecific type and how animals may alter behavior accordingly is not well known. We examined whether the communally breeding spiny mouse (Acomys cahirinus) responds differently to conspecifics that vary in novelty and kinship. In a group interaction test, we found that males can distinguish novel kin from novel non-kin, and preferentially spend time with novel kin over familiar kin and novel non-kin. To determine whether kinship and novelty status are differentially represented in the brain, we conducted immediate early gene tests, which revealed the dorsal, but not ventral, lateral septum differentially processes kinship. Neither region differentially processes social novelty. Further, males did not exhibit differences in prosocial behavior toward novel and familiar conspecifics but exhibited more prosocial behavior with novel kin than novel non-kin. These results suggest that communally breeding species may have evolved specialized neural circuitry to facilitate a bias to be more affiliative with kin, regardless of whether they are novel or familiar, potentially to promote prosocial behaviors, thereby facilitating group cohesion. 
    more » « less
  2. Social experiences can shape adult behavior and cognition. Here, we use El Abra swordtails (Xiphophorus nigrensis) to assess how life-long experience with different male mating tactics shapes coercion evasion ability and female spatial cognition. We raised females from birth to adulthood in environments that varied by male mating tactic: coercers only, courtship displayers only, coercers and displayers together, mixed-strategists, and female only. In adulthood, we tested females’ behavioral responses to a coercive male and spatial cognition in a maze. Females reared with only displayers were significantly worse at distancing themselves from the coercive male than females raised with coercers and displayers and females raised with only coercers. Females raised with a single mating tactic (either courtship display or coercion) exhibited significantly higher accuracy in the spatial maze than females from other rearing groups, and showed significant reduction in total errors (courtship display group) or latency to reward (coercion group) over successive trials. These more predictable environments (one tactic), and not the more complex environments (two tactics), showed evidence for spatial learning. The results are discussed in light of the existing literature on two components of environmental change (environmental predictability and the certainty with which cues predict the best behavioral response) and their effect on the development of cognitive abilities. 
    more » « less
  3. Abstract Transmission of maternal behavior across generations occurs, but less is known about paternal behavior. In biparental species like the California mouse (Peromyscus californicus), paternal care contributes to the well‐being of offspring with lasting consequences on the brain and behavior. Paternal huddling/grooming behavior can be passed on to future generations, but whether paternal retrieval, which removes young from potential harm, is transmitted independently is unclear. We manipulated paternal retrieval experience through pup displacement manipulations, then examined whether males exposed to higher levels of paternal retrieval in development altered their adult retrieval behavior with their offspring. Males exposed to heightened paternal retrievals, as compared to reduced retrievals, retrieved their offspring more often but huddled/groomed offspring less during undisturbed natural observations. No differences were observed following a pup displacement challenge. The high paternal retrieval group also exhibited more physical activity and stereotypy. Our results are consistent with the hypothesis that paternal retrieval levels are transmitted across generations and may function via mechanisms separate from huddling/grooming. One modifying factor may be anxiety because increased activity and stereotypy occurred in the high retrieval group. We speculate how the transmission of paternal retrievals may inform a protective parenting style. 
    more » « less
  4. null (Ed.)
    Abstract Background How the brain develops accurate models of the external world and generates appropriate behavioral responses is a vital question of widespread multidisciplinary interest. It is increasingly understood that brain signal variability—posited to enhance perception, facilitate flexible cognitive representations, and improve behavioral outcomes—plays an important role in neural and cognitive development. The ability to perceive, interpret, and respond to complex and dynamic social information is particularly critical for the development of adaptive learning and behavior. Social perception relies on oxytocin-regulated neural networks that emerge early in development. Methods We tested the hypothesis that individual differences in the endogenous oxytocinergic system early in life may influence social behavioral outcomes by regulating variability in brain signaling during social perception. In study 1, 55 infants provided a saliva sample at 5 months of age for analysis of individual differences in the oxytocinergic system and underwent electroencephalography (EEG) while listening to human vocalizations at 8 months of age for the assessment of brain signal variability. Infant behavior was assessed via parental report. In study 2, 60 infants provided a saliva sample and underwent EEG while viewing faces and objects and listening to human speech and water sounds at 4 months of age. Infant behavior was assessed via parental report and eye tracking. Results We show in two independent infant samples that increased brain signal entropy during social perception is in part explained by an epigenetic modification to the oxytocin receptor gene ( OXTR ) and accounts for significant individual differences in social behavior in the first year of life. These results are measure-, context-, and modality-specific: entropy, not standard deviation, links OXTR methylation and infant behavior; entropy evoked during social perception specifically explains social behavior only; and only entropy evoked during social auditory perception predicts infant vocalization behavior. Conclusions Demonstrating these associations in infancy is critical for elucidating the neurobiological mechanisms accounting for individual differences in cognition and behavior relevant to neurodevelopmental disorders. Our results suggest that an epigenetic modification to the oxytocin receptor gene and brain signal entropy are useful indicators of social development and may hold potential diagnostic, therapeutic, and prognostic value. 
    more » « less
  5. Parental effects, or parental phenotypes affecting offspring phenotypes, are widespread across taxa, yet there is significant variation within species regarding which offspring traits are affected. One reason for this observed variation could be the type of sensory cues present in the parental environment. By exposing parents to sensory cues containing different information about the same ecological stressor, we can determine whether information is integrated differently by parents based on cue type, leading to differential trait development in offspring. In this study, we utilized predator cues, which can be found in isolation and in combination in natural settings, to test whether cue type plays a role in differential phenotype expression in Trinidadian guppies, Poecilia reticulata. Parents were exposed to predator cues (visual, olfactory or both combined) over 14 days, after which we assessed life history traits, morphology and activity. Offspring were then raised with no predator cues and tested for morphology and activity in adulthood. No differences in life history traits were observed across 10 weeks. In line with previous findings, behaviour differed in both the parent and F1 generations in response to predator cues; however, effects were dependent on cue type and sex. Our results suggest that exposure to even a single sensory cue is strong enough to initiate a cascade of responses both in parent and F1 generations, and that interacting factors such as cue type and sex lend importance to understanding consequences of parent risk perception for offspring. 
    more » « less