Current Biology
Volume 30, Issue 18, 21 September 2020, Pages 3647-3656.e3
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Rapid Effects of Selection on Brain-wide Activity and Behavior

https://doi.org/10.1016/j.cub.2020.06.086Get rights and content
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Highlights

  • ASR habituation-selected zebrafish larvae differ in whole-brain activity patterns

  • Low habituation selection leads to increased activity in ASR circuits at baseline

  • High habituation selection increases activity in HC dopamine neurons

  • Selected animals differ in swim activity as larvae and stress responses as adults

Summary

Interindividual variation in behavior and brain activity is universal and provides substrates for natural selection [1, 2, 3, 4, 5, 6, 7, 8, 9]. Selective pressures shift the expression of behavioral traits at the population level [10, 11], but the accompanying changes of the underlying neural circuitry have rarely been identified [12, 13]. Selection likely acts through the genetic and/or epigenetic underpinnings of neural activity controlling the selected behavior [14]. Endocrine and neuromodulatory systems participate in behavioral diversity and could provide the substrate for evolutionary modifications [15, 16, 17, 18, 19, 20, 21]. Here, we examined brain-wide patterns of activity in larval zebrafish selectively bred over two generations for extreme differences in habituation of the acoustic startle response (ASR) [22]. The ASR is an evolutionarily conserved defensive behavior induced by strong acoustic/vibrational stimuli. ASR habituation shows great individual variability that is stable over days and heritable [4, 22]. Selection for high ASR habituation leads to stronger sound-evoked activation of ASR-processing brain areas. In contrast, animals selected for low habituation displayed stronger spontaneous activity in ASR-processing centers. Ablation of dopaminergic tyrosine hydroxylase (TH) neurons decreased ASR sensitivity. Independently selected ASR habituation lineages link the effect of behavioral selection to dopaminergic caudal hypothalamus (HC) neurons [23]. High ASR habituation co-segregated with decreased spontaneous swimming phenotypes, but visual startle responses were unaffected. Furthermore, high- and low-habituation larvae differed in stress responses as adults. Thus, selective pressure over a couple of generations on ASR habituation behavior is able to induce substantial differences in brain activity, carrying along additional behaviors as piggyback traits that might further affect fitness in the wild.

Keywords

zebrafish
individuality
brain evolution
behavioral selection
neuromodulation
startle

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