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Slow to warm up: the role of habituation in social fear.

ABSTRACT: Neural habituation allows familiar information to be ignored in favor of salient or novel stimuli. In contrast, failure to rapidly habituate likely reflects deficits in the ability to learn that an environment is predictable, familiar and safe. Differences in habituation rate may underlie individual differences in the tendency to approach or avoid novelty; however, many questions remain unanswered. Given the importance of adaptive social functioning, here we tested whether habituation differences to social stimuli are associated with differences in social fearfulness, a trait that ranges from low social fear-the adaptive tendency to approach novel social stimuli-to high social fear-the maladaptive tendency to avoid novel social stimuli. Higher social fearfulness was associated with slower habituation across regions of the social brain, including the hippocampus, amygdala, ventromedial prefrontal cortex, medial orbitofrontal cortex, fusiform face area, primary visual cortex, and extrastriate visual cortex. Interestingly, habituation differences were driven by sustained amygdala-visual cortex interactions, but not deficient amygdala-prefrontal cortex interactions. Together, these findings provide evidence that a failure to filter social stimuli is associated with a key social trait. In light of the link between social fear and dysfunction, individual differences in habituation may provide an important neurobiological marker for risk for psychiatric illness, such as social anxiety disorder.

SUBMITTER: Avery SN

PROVIDER: S-EPMC5091686 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Slow to warm up: the role of habituation in social fear.

Avery Suzanne N SN Blackford Jennifer Urbano JU

Social cognitive and affective neuroscience 20160721 11

Neural habituation allows familiar information to be ignored in favor of salient or novel stimuli. In contrast, failure to rapidly habituate likely reflects deficits in the ability to learn that an environment is predictable, familiar and safe. Differences in habituation rate may underlie individual differences in the tendency to approach or avoid novelty; however, many questions remain unanswered. Given the importance of adaptive social functioning, here we tested whether habituation difference ...[more]

PMID: 27445209

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Project description:In most aphid species, facultative parthenogenetic reproduction allows rapid growth and formation of large single-genotype colonies. Upon predator attack, individual aphids emit an alarm pheromone to warn the colony of this danger. (E)-beta-farnesene (EBF) is the predominant constituent of the alarm pheromone in Myzus persicae (green peach aphid) and many other aphid species. Continuous exposure to alarm pheromone in aphid colonies raised on transgenic Arabidopsis thaliana plants that produce EBF leads to habituation of the aphid population. Whereas naïve aphids are repelled by EBF, habituated aphids show no avoidance response. Individual aphids from the habituated colony can revert back to being EBF-sensitive in three generations, indicating that this behavioral change is not caused by a genetic mutation. Instead, DNA microarray experiments comparing gene expression in naïve and habituated aphids treated with EBF demonstrate an almost complete desensitization in the transcriptional response to EBF. Furthermore, EBF-responsive aphids, but not habituated aphids show significantly lower reproduction in the presence of EBF. Although both naïve and habituated aphids emit EBF upon damage, EBF-responsive aphids display a higher survival rate in the presence of coccinellid predators and thus outperform habituated aphids that do not show an avoidance response. These results provide direct evidence that aphid perception of conspecific alarm pheromone aids in predator avoidance and thereby bestows fitness benefits in survivorship and fecundity. Although habituated M. persicae have equal fecundity on control and EBF-producing plants, such transgenics may have practical applications in agriculture because of increased predation of habituated aphids. Log fold-changes (LogFC) were computed and contigs with P-values ≤ 0.05 were considered to be differentially expressed (see Supplementary file at foot of this record). Agilent 8x15K array previously reported by Ramsey et al., 2007 - BMC Genomics 8: 243. Two-condition experiment using Alexa Fluor 555 and 647 dyes. Biological replicates: 4 control replicates, 4 treated replicates.

Project description:A fundamental tenet of maternal effects assumes that maternal variance over time should have discordant consequences for offspring traits across litters. Yet, seldom are parents observed across multiple reproductive bouts, with few studies considering anthropogenic disturbances as an ecological driver of maternal effects. We observed captive coyote (Canis latrans) pairs over two successive litters to determine whether among-litter differences in behavior (i.e., risk-taking) and hormones (i.e., cortisol and testosterone) corresponded with parental plasticity in habituation. Thus, we explicitly test the hypothesis that accumulating experiences of anthropogenic disturbance reduces parental fear across reproductive bouts, which should have disparate phenotypic consequences for first- and second-litter offspring. To quantify risk-taking behavior, we used foraging assays from 5-15 weeks of age with a human observer present as a proxy for human disturbance. At 5, 10, and 15 weeks of age, we collected shaved hair to quantify pup hormone levels. We then used a quantitative genetic approach to estimate heritability, repeatability, and between-trait correlations. We found that parents were riskier (i.e., foraged more frequently) with their second versus first litters, supporting our prediction that parents become increasingly habituated over time. Second-litter pups were also less risk-averse than their first-litter siblings. Heritability for all traits did not differ from zero (0.001-0.018); however, we found moderate support for repeatability in all observed traits (r = 0.085-0.421). Lastly, we found evidence of positive phenotypic and cohort correlations among pup traits, implying that cohort identity (i.e., common environment) contributes to the development of phenotypic syndromes in coyote pups. Our results suggest that parental habituation may be an ecological cue for offspring to reduce their fear response, thus emphasizing the role of parental plasticity in shaping their pups' behavioral and hormonal responses toward humans.

Dataset Information

Slow to warm up: the role of habituation in social fear.

Publications

Slow to warm up: the role of habituation in social fear.

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