Abstract

Aggregation is a defensive strategy employed by many prey species in response to predatory threat. Our group has characterized defensive aggregation (huddling) in Rattus norvegicus in response to a ball of cat fur. In this situation some rats huddle less, and approach the threatening cue more than others (active vs. passive responders). The present study explored whether active responding is a stable phenotype associated with behaviors outside direct predatory encounters. The neural substrates of active and passive responding under predatory threat were explored using c-Fos immunohistochemistry. Finally, we examined whether the presence of conspecifics during predatory threat biases behavior towards active responding. Active and passive responding styles were found to be stable in individual rats across consecutive group exposures to cat fur, and were predicted by anxiety-like behavior in an open-field emergence test. Active responders displayed less conditioned fear in an environment associated with predatory threat, and had higher post-exposure intake of a weak sucrose solution (a test of “anhedonia”). Active responding was associated with: greater cat fur-induced activation of the accessory olfactory bulb, reflecting greater olfactory stimulation in rats actively approaching the fur; lowered activation of somatosensory cortex, reflecting reduced huddling with conspecifics; and reduced activation in the lateral septum. Social exposure to cat fur promoted active responding relative to individual exposure, and lowered c-Fos expression in the dorsomedial periaqueductal grey, medial caudate putamen and lateral habenula. We conclude that individual differences in anti-predator behavior appear stable traits with active responders having a more resilient phenotype. Social exposure to predatory threat has an acute buffering effect, subtly changing the neural and behavioral response towards threat and encouraging active responding. An association between active responding and lower c-Fos expression in the lateral septum is consistent with previous studies that highlight this region as an important neurobiological substrate of defensive aggregation.

Highlights

  • Defensive aggregation is a ubiquitous response in prey species involving the tight grouping of animals in response to predatory threat

  • Defensive aggregation is observed across a wide array of mammalian and non-mammalian species [1], for example: Emperor Penguins [2]; the marine insect Halobates robustus [3]; and Serengeti ungulates such as wildebeest, zebra, and Thomson’s gazelle [4]

  • This does not occur, when only two rats are present [13]. Such results are predicted by the dilution effect, which sees the survival benefit afforded by aggregation as increasing with the size of the group, through a decrease in the probability that any individual animal will be attacked [3,15]

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Summary

Introduction

Defensive aggregation is a ubiquitous response in prey species involving the tight grouping (e.g. huddling, flocking or shoaling) of animals in response to predatory threat. The response of groups of laboratory rats to predatory threat was first described by Blanchard & Blanchard [12] using a laboratory ‘‘visible burrow system’’ These authors reported hasty retreat and a subsequent increase in non-sexual, non-aggressive social contacts in the burrow system when rats encountered a live cat at the burrow surface. In more recent work [13,14], our group has described high levels of huddling when groups of four cage mates are exposed to cat fur in an open arena. This does not occur, when only two rats are present [13]. Such results are predicted by the dilution effect, which sees the survival benefit afforded by aggregation as increasing with the size of the group, through a decrease in the probability that any individual animal will be attacked [3,15]

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