Social cues shift functional connectivity in the hypothalamus

Abstract

We determined how social stimuli that vary in behavioral relevance differentially activate functional networks in the frog hypothalamus. As measured by egr-1 mRNA levels, activity in three hypothalamic nuclei varied with acoustic stimulus, and these responses were correlated with egr-1 responses in different auditory regions regardless of stimulus. The correlations among hypothalamic nuclei, however, varied as a function of the behavioral relevance of the stimuli. Thus relevant social cues shift the functional connectivity within the hypothalamus, consistent with principles that underlie the simultaneous processing of sensory information in cognitive tasks.amphibian ͉ immediate early gene ͉ mate choice ͉ neural network ͉ tú ngara frog T he complex anatomical connections characteristic of networks in the brain pose a challenge for understanding neural circuits and their dual capacities to motivate and respond to behavior. A traditional approach in studies of neural systems underlying social behavior has been to investigate properties of individual nuclei or centers. Alternatively, cognitive neuroscience studies have more recently focused on variation in the functional relationships among neocortical areas, that is, on network properties indicated by correlated patterns of activity among brain regions, or functional connectivity (1-3). Functional connectivity has been assessed by using metabolic measures such as positron emission tomography (1) or fluorodeoxyglucose incorporation (4) to infer neural activity patterns within brain networks.The limbic and hypothalamic areas are critical candidates for network analyses, because those nuclei are heavily and reciprocally interconnected anatomically and participate in complex ways in multiple aspects of behavior and physiology (5). The brain directs appropriate behavioral and physiological responses to diverse sensory inputs by partitioning interconnected brain regions into independent subnetworks that subserve different tasks (5). Newman (5) described the flexibility of functional connections involved in a variety of aggressive, sexual, and maternal behaviors in the context of a social behavior network of six limbic regions. A similar but not entirely congruent network of limbic regions has been described in geckos (6) in which developmental influences on functional connectivity have been linked to aggressive behaviors (7). Newman (5) predicted that sensory inputs modulate the transient subnetworks that mediate continuously varying behavioral responses to social cues. In this paper, we extend Newman's prediction to consider how socially relevant auditory inputs demarcate subnetworks in the hypothalamus, a brain division that has a critical role in mediating reproductive responses to social cues.Anurans are tractable models for such an investigation. Behavioral responses to conspecific vocal signals are well documented, and we have a rich understanding of how the auditory system differentially responds to behaviorally relevant acoustic stimuli (8,9). Neuroanatomical con...

Effects of season, testosterone and female exposure on c-fos expression in the preoptic area and amygdala of male green anoles

“…Also, c-fos expression is increased in rodents when males and females are housed together, thus experiencing social contact, compared to isolated counterparts (Schwab et al, 2004). In contrast to the present results, immediate early gene expression is increased in specific regions of the hypothalamus and suprachiasmatic nucleus of the female frog forebrain after hearing a socially relevant call compared to those hearing no sound or irrelevant calls (Hoke et al, 2005). However, similar to our results, immediate early gene expression in the POA in these frogs did not differ between groups receiving social stimuli compared to those that did not.…”

“…In addition, it is possible that other types of POA and AMY neurons are active. They may express proteins other than c-fos (Bailey and Wade, 2003;Hoffman and Lyo, 2002;Hoke et al, 2005), or other biochemical markers of changes in neuronal activity (Tlemçani et al, 2000) might show relationships between that were not detected in the present study. This and previous work in the green anole POA and AMY suggest that T, and potentially AR, increases motivation and expression of masculine sexual behaviors by enhancing soma size and diminishing c-fos expression.…”

Social regulation of plasma estradiol concentration in a female anuran

“…This is possible because in anurans, the central auditory system sends projections into the anterior and central thalamic nuclei, which relay auditory information into the anterior preoptic area as well as the ventral hypothalamus (reviewed in Wilczynski et al, 1993). Consequently, hypothalamic neurons respond to acoustic stimulation in male (Wilczynski and Allison, 1989;Allison, 1992) and female (Hoke et al, 2005) anurans. Acoustic cues stimulate the release of gonadal hormones in male anuran amphibians (Burmeister and Wilczynski, 2000;Chu and Wilczynski, 2001).…”

Neural control of gene recruitment in metazoans

“…Females use an intricate way to achieve this result: they encode sound waves of the song in the auditory apparatus of the brain (Hoke et al, 2005) in the form of trains of electrical signals and send them for processing into a complex neurobiological maze with the final output leading to expression of the gene egr-1 and a modification of neuronal connections in the hypothalamus (Almli and Wilczynski, 2009) that by means of the hypothalamic-pituitary-ovarian axis leads to increased estradiol synthesis and secretion. The reason why only tú ngara frogs express the egr-1 gene in their brains, although other frog species have the same gene is because tú ngara frogs alone have evolved the capability to generate the chemical output necessary for expressing the egr-1 gene in relevant neurons in the brain by processing the species-specific male call in particular neural circuits.…”