Experience, circuit dynamics, and forebrain recruitment in larval zebrafish prey capture

Abstract

Experience strongly influences behavior, but little is known about how experience is encoded in the brain, and how changes in neural activity are implemented at a network level to improve performance. Here we investigate how differences in experience impact brain circuitry and behavior in larval zebrafish prey capture. We find that experience of live prey compared to inert food increases capture success by boosting capture initiation. To explore the underlying neural basis, we studied the effects of prior experience of live prey on behavior and brain activity. In response to live prey, animals with and without prior experience of live prey all show activity in visual areas (pretectum and optic tectum) and motor areas (cerebellum and hindbrain), with similar visual area retinotopic maps of prey position. However, prey-experienced animals more readily initiate capture in response to visual area activity and also have greater visually-evoked activity in two forebrain areas: the telencephalon and the habenula. Consistent with the contribution of the forebrain to prey capture, disruption of neurons in the habenula reduced prey capture performance in prey-experienced fish. Together, our results suggest that experience of prey strengthens prey-associated visual drive to the forebrain, and that this lowers the threshold for prey-associated visual activity to trigger activity in motor areas, thereby improving capture performance.

fmr1mutation interacts with sensory experience to alter the early development of behavior and sensory coding in zebrafish

“…This could potentially place fish raised under naturalistic conditions at a disadvantage in our prey capture assay, since they have adapted to hunting in a richer visual environment than the reduced stimulation case. This would be potentially analogous to recent reports that whether zebrafish first experience dry or live food influences their subsequent behavior and brain development [64, 65].…”

In vivo calcium imaging reveals disordered interictal network dynamics in epileptic stxbp1b zebrafish

“…Heterozygous stxbp1b fish were generated by clustered regularly interspaced short palindromic repeats (CRISPR)-mediated knockout, as described ( Grone et al., 2016 ) and in-crossed with transgenic zebrafish expressing neuronal-specific GCaMP6f [ Tg (neurod1:GCaMP6f) line] ( Rupprecht et al., 2016 ). This unique transgenic neurod1 :GCaMPf line was developed for fast calcium imaging studies in larval zebrafish ( Oldfield et al., 2020 ). Pigment-free nacre ( mitfa -/- ) offspring with GCaMP6f expression were sorted on 4 days post fertilization (dpf) and used for calcium imaging experiments on 5-7 dpf.…”

Neuromodulation and Behavioral Flexibility in Larval Zebrafish: From Neurotransmitters to Circuits

“…Moreover, compared to controls, prey-experienced fish had higher visually-evoked neuronal activity in the telencephalon and the habenula, suggesting that the two brain structures may contain neurons regulating learning processes required for refining motor sequences involved in hunting behavior (Oldfield et al, 2020). In support of this hypothesis, the ablation of habenular neurons led to a reduction of capture efficiency (Oldfield et al, 2020). More work is needed to identify the precise forebrain circuits responsible for this form of learning.…”

“…In accord with these latter reports, it was shown that learning is involved in prey-capture behavior performed by young fish. Larvae exposed to live prey (paramecia or rotifers) displayed elevated capture success compared to naïve larvae or controls raised with inert food (Lagogiannis et al, 2020;Oldfield et al, 2020). Moreover, compared to controls, prey-experienced fish had higher visually-evoked neuronal activity in the telencephalon and the habenula, suggesting that the two brain structures may contain neurons regulating learning processes required for refining motor sequences involved in hunting behavior (Oldfield et al, 2020).…”

“…Larvae exposed to live prey (paramecia or rotifers) displayed elevated capture success compared to naïve larvae or controls raised with inert food (Lagogiannis et al, 2020;Oldfield et al, 2020). Moreover, compared to controls, prey-experienced fish had higher visually-evoked neuronal activity in the telencephalon and the habenula, suggesting that the two brain structures may contain neurons regulating learning processes required for refining motor sequences involved in hunting behavior (Oldfield et al, 2020). In support of this hypothesis, the ablation of habenular neurons led to a reduction of capture efficiency (Oldfield et al, 2020).…”