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.

Leveraging individual power to improve racial equity in academia.

Academia in the United States continues to grapple with its longstanding history of racial discrimination and its active perpetuation of racial disparities. To this end, universities and academic societies must grow in ways that reduce racial minoritization and foster racial equity. What are the effective and long-lasting approaches we as academics should prioritize to promote racial equity in our academic communities? To address this, the authors held a diversity, equity, and inclusion (DEI) panel during the Society for Behavioral Neuroendocrinology 2022 annual meeting, and in the following commentary synthesize the panelists' recommendations for fostering racial equity in the US academic community.

A test of the social behavior network reveals differential patterns of neural responses to social novelty in bonded, but not non-bonded, male prairie voles.

The social behavior network (SBN) has provided a framework for understanding the neural control of social behavior. The original SBN hypothesis proposed this network modulates social behavior and should exhibit distinct patterns of neural activity across nodes, which correspond to distinct social contexts. Despite its tremendous impact on the field of social neuroscience, no study has directly tested this hypothesis. Thus, we assessed Fos responses across the SBN of male prairie voles (Microtus ochrogaster). Virgin/non-bonded and pair bonded subjects were exposed to a sibling cagemate or pair bonded partner, novel female, novel male, novel meadow vole, novel object, or no stimulus. Inconsistent with the original SBN hypothesis, we did not find profoundly different patterns of neural responses across the SBN for different contexts, but instead found that the SBN generated significantly different patterns of activity in response to social novelty in pair bonded, but not non-bonded males. These findings suggest that non-bonded male prairie voles may perceive social novelty differently from pair bonded males or that SBN functionality undergoes substantial changes after pair bonding. This study reveals novel information about bond-dependent, context-specific neural responsivity in male prairie voles and suggests that the SBN may be particularly important for processing social salience. Further, our study suggests there is a need to reconceptualize the framework of how the SBN modulates social behavior.

Distribution of vasopressin 1a and oxytocin receptor protein and mRNA in the basal forebrain and midbrain of the spiny mouse (Acomys cahirinus).

The nonapeptide system modulates numerous social behaviors through oxytocin and vasopressin activation of the oxytocin receptor (OXTR) and vasopressin receptor (AVPR1A) in the brain. OXTRs and AVPR1As are widely distributed throughout the brain and binding densities exhibit substantial variation within and across species. Although OXTR and AVPR1A binding distributions have been mapped for several rodents, this system has yet to be characterized in the spiny mouse (Acomys cahirinus). Here we conducted receptor autoradiography and in situ hybridization to map distributions of OXTR and AVPR1A binding and Oxtr and Avpr1a mRNA expression throughout the basal forebrain and midbrain of male and female spiny mice. We found that nonapeptide receptor mRNA is diffuse throughout the forebrain and midbrain and does not always align with OXTR and AVPR1A binding. Analyses of sex differences in brain regions involved in social behavior and reward revealed that males exhibit higher OXTR binding densities in the lateral septum, bed nucleus of the stria terminalis, and anterior hypothalamus. However, no association with gonadal sex was observed for AVPR1A binding. Hierarchical clustering analysis further revealed that co-expression patterns of OXTR and AVPR1A binding across brain regions involved in social behavior and reward differ between males and females. These findings provide mapping distributions and sex differences in nonapeptide receptors in spiny mice. Spiny mice are an excellent organism for studying grouping behaviors such as cooperation and prosociality, and the nonapeptide receptor mapping here can inform the study of nonapeptide-mediated behavior in a highly social, large group-living rodent.

Protocol for multiplex fluorescent immunohistochemistry in free-floating rodent brain tissues.

Identifying multiple proteins within the same tissue allows for assessing protein colocalization, is cost effective, and maximizes efficiency. Here, we describe a protocol for multiplex immunolabeling of proteins in free-floating rodent brain sections. As opposed to slide-mounted immunohistochemistry, the free-floating approach results in less tissue loss and greater antibody penetration. Using distinct fluorophores for individual proteins, this protocol allows for visualization of three or more proteins within tissue sections. The protocol can be applied to other tissue types. For complete details on the use and execution of this protocol, please refer to Gonzalez Abreu et al. (2022).

Species-typical group size differentially influences social reward neural circuitry during nonreproductive social interactions.

We investigated whether nonreproductive social interactions may be rewarding for colonial but not non-colonial species. We found that the colonial spiny mouse (Acomys cahirinus) is significantly more gregarious, more prosocial, and less aggressive than its non-colonial relative, the Mongolian gerbil (Meriones unguiculatus). In an immediate-early gene study, we examined oxytocin (OT) and tyrosine hydroxylase (TH) neural responses to interactions with a novel, same-sex conspecific or a novel object. The paraventricular nucleus of the hypothalamus (PVN) OT cell group was more responsive to interactions with a conspecific compared to a novel object in both species. However, the ventral tegmental area (VTA) TH cell group showed differential responses only in spiny mice. Further, PVN OT and VTA TH neural responses positively correlated in spiny mice, suggesting functional connectivity. These results suggest that colonial species may have evolved neural mechanisms associated with reward in novel, nonreproductive social contexts to promote large group-living.

Social ascent changes cognition, behaviour and physiology in a highly social cichlid fish.

When an individual ascends in dominance status within their social community, they often undergo a suite of behavioural, physiological and neuromolecular changes. While these changes have been extensively characterized across a number of species, we know much less about the degree to which these changes in turn influence cognitive processes like associative learning, memory and spatial navigation. Here, we assessed male Astatotilapia burtoni, an African cichlid fish known for its dynamic social dominance hierarchies, in a set of cognitive tasks both before and after a community perturbation in which some individuals ascended in dominance status. We assayed steroid hormone (cortisol, testosterone) levels before and after the community experienced a social perturbation. We found that ascending males changed their physiology and novel object recognition preference during the perturbation, and they subsequently differed in social competence from non-ascenders. Additionally, using a principal component analysis we were able to identify specific cognitive and physiological attributes that appear to predispose certain individuals to ascend in social status once a perturbation occurs. These previously undiscovered relationships between social ascent and cognition further emphasize the broad influence of social dominance on animal decision-making. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Decision-making in a social world: Integrating cognitive ecology and social neuroscience.

Understanding animal decision-making involves simultaneously dissecting and reconstructing processes across levels of biological organization, such as behavior, physiology, and brain function, as well as considering the environment in which decisions are made. Over the past few decades, foundational breakthroughs originating from a variety of model systems and disciplines have painted an increasingly comprehensive picture of how individuals sense information, process it, and subsequently modify behavior or states. Still, our understanding of decision-making in social contexts is far from complete and requires integrating novel approaches and perspectives. The fields of social neuroscience and cognitive ecology have approached social decision-making from orthogonal perspectives. The integration of these perspectives (and fields) is critical in developing comprehensive and testable theories of the brain.

Equal performance but distinct behaviors: sex differences in a novel object recognition task and spatial maze in a highly social cichlid fish.

Sex differences in behavior and cognition can be driven by differential selection pressures from the environment and in the underlying neuromolecular mechanisms of decision-making. The highly social cichlid fish Astatotilapia burtoni exhibits dynamic and complex social hierarchies, yet explicit cognitive testing (outside of social contexts) and investigations of sex differences in cognition have yet to be fully explored. Here we assessed male and female A. burtoni in two cognitive tasks: a novel object recognition task and a spatial task. We hypothesized that males outperform females in a spatial learning task and exhibit more neophilic/exploratory behavior across both tasks. In the present study we find that both sexes prefer the familiar object in a novel object recognition task, but the time at which they exhibit this preference differs between the sexes. Females more frequently learned the spatial task, exhibiting longer decision latencies and quicker error correction, suggesting a potential speed-accuracy tradeoff. Furthermore, the sexes differ in space use in both tasks and in a principal component analysis of the spatial task. A model selection analysis finds that preference, approach, and interaction duration in the novel object recognition task reach a threshold of importance averaged across all models. This work highlights the need to explicitly test for sex differences in cognition to better understand how individuals navigate dynamic social environments.

A systems change framework for evaluating academic equity and inclusion in an Ecology and Evolution Graduate Program.

While academia is moving forward in terms of diversifying recruitment of undergraduate and graduate students, diverse representation is still not found across the academic hierarchy. At the graduate level, new discussions are emerging around efforts to improve the experiences of women and underrepresented minorities through inclusive graduate programming. Inclusive graduate programs are that which actively center and prioritize support for diverse experiences, identities, career goals, and perspectives, from recruitment through graduation. Establishing regular and rigorous evaluation of equity and inclusion efforts and needs is a critical component of this work. This is recognized by funding agencies that increasingly require reporting on inclusion efforts; here, we suggest use of a systems change framework for these evaluations. A systems change approach emphasizes three levels: explicit change (e.g., policies), semi-explicit change (e.g., power dynamics), and implicit change (e.g., biases). We use the Ecology, Evolution, and Behavior (EEB) PhD Program at the University of Texas at Austin in an exercise to (a) identify areas of concern regarding inclusive programming voiced by graduate students, (b) categorize efforts to address these concerns, and (c) integrating and evaluating which areas of the systems change framework show the greatest progress or potential for progress. We argue this framework is particularly useful for academic systems as they are complex, composed of variable individuals, and must address diverse stakeholder needs.

Sex differences in cognitive performance and style across domains in mosquitofish (Gambusia affinis).

Given that the sexes often differ in their ecological and sexual selection pressures, sex differences in cognitive properties are likely. While research on sexually dimorphic cognition often focuses on performance, it commonly overlooks how sexes diverge across cognitive domains and in behaviors exhibited during a cognitive task (cognitive style). We tested male and female western mosquitofish (Gambusia affinis) in three cognitive tasks: associative learning (numerical discrimination), cognitive flexibility (detour task), and spatio-temporal learning (shuttlebox). We characterized statistical relationships between cognitive performances and cognitive style during the associative learning task with measures of anxiety, boldness, exploration, reaction time, and activity. We found sex differences in performance, cognitive style, and the relationships between cognitive domains. Females outperformed males in the spatio-temporal learning task, while the sexes performed equally in associate learning and cognitive flexibility assays. Females (but not males) exhibited a 'fast-exploratory' cognitive style during associative learning trials. Meanwhile, only males showed a significant positive relationship between domains (associative learning and cognitive flexibility). We propose that these sexually dimorphic cognitive traits result from strong sexual conflict in this taxon; and emphasize the need to explore suites of sex-specific cognitive traits and broader comparative work examining sexual selection and cognition.

Cryptic sexual dimorphism in spatial memory and hippocampal oxytocin receptors in prairie voles (Microtus ochrogaster).

Sex differences are well documented and are conventionally associated with intense sex-specific selection. For example, spatial memory is frequently better in males, presumably due to males' tendency to navigate large spaces to find mates. Alternatively, monogamy (in which sex-specific selection is relatively relaxed) should diminish or eliminate differences in spatial ability and the mechanisms associated with this behavior. Nevertheless, phenotypic differences between monogamous males and females persist, sometimes cryptically. We hypothesize that sex-specific cognitive demands are present in monogamous species that will influence neural and behavioral phenotypes. The effects of these demands should be observable in spatial learning performance and neural structures associated with spatial learning and memory. We analyzed spatial memory performance, hippocampal volume and cell density, and hippocampal oxytocin receptor (OTR) expression in the socially monogamous prairie vole. Compared to females, males performed better in a spatial memory and spatial learning test. Although we found no sex difference in hippocampal volume or cell density, male OTR density was significantly lower than females, suggesting that performance may be regulated by sub-cellular mechanisms within the hippocampus that are less obvious than classic neuroanatomical features. Our results suggest an expanded role for oxytocin beyond facilitating social interactions, which may function in part to integrate social and spatial information.

Specific, sensitive, and quantitative enzyme-linked immunosorbent assay for human immunoglobulin G antibodies to anthrax toxin protective antigen.

The bioterrorism-associated human anthrax epidemic in the fall of 2001 highlighted the need for a sensitive, reproducible, and specific laboratory test for the confirmatory diagnosis of human anthrax. The Centers for Disease Control and Prevention developed, optimized, and rapidly qualified an enzyme-linked immunosorbent assay (ELISA) for immunoglobulin G (IgG) antibodies to Bacillus anthracis protective antigen (PA) in human serum. The qualified ELISA had a minimum detection limit of 0.06 micro g/mL, a reliable lower limit of detection of 0.09 micro g/mL, and a lower limit of quantification in undiluted serum specimens of 3.0 micro g/mL anti-PA IgG. The diagnostic sensitivity of the assay was 97.8%, and the diagnostic specificity was 97.6%. A competitive inhibition anti-PA IgG ELISA was also developed to enhance diagnostic specificity to 100%. The anti-PA ELISAs proved valuable for the confirmation of cases of cutaneous and inhalational anthrax and evaluation of patients in whom the diagnosis of anthrax was being considered.