Zebrafish Exploit Visual Cues and Geometric Relationships to Form a Spatial Memory

Abstract

Animals use salient cues to navigate in their environment, but their specific cognitive strategies are largely unknown. We developed a conditioned place avoidance paradigm to discover whether and how zebrafish form spatial memories. In less than an hour, juvenile zebrafish, as young as 3 weeks, learned to avoid the arm of a Y-maze that was cued with a mild electric shock. Interestingly, individual fish solved this task in different ways: by staying in the safe center of the maze or by preference for one, or both, of the safe arms. In experiments in which the learned patterns were swapped, rotated, or replaced, the animals could transfer the association of safety to a different arm or to a different pattern using either visual cues or location as the conditioned stimulus. These findings show that juvenile zebrafish exhibit several complementary spatial learning modes, which generate a flexible repertoire of behavioral strategies.

Functional properties of habenular neurons are determined by developmental stage and sequential neurogenesis

“…In turn, such a developmental order would contribute to an increased diversity of habenular neurons across development. Several recent studies suggest that complex and cognitively demanding behaviours arise later in development as animals maturate (Amo et al, 2014;Andalman et al, 2019;Valente et al, 2012;Yashina et al, 2019). Our findings in habenula suggest that such expansion of animal behaviour might be due to incorporation of new functional modules at different developmental time points.…”

“…In this study we investigated the functional development of habenular circuits across multiple developmental stages of zebrafish from relatively simpler larvae to juvenile zebrafish with complex behaviours (Amo et al, 2014;Andalman et al, 2019;Chou et al, 2016;Dreosti et al, 2015;Hinz and de Polavieja, 2017;Ksenia Yashina, 2019;Valente et al, 2012). The use of juvenile zebrafish is getting increasingly popular due to their transparent brains and expanded behavioural repertoire that requires habenular function (Andalman et al, 2019;Dreosti et al, 2015;Hinz and de Polavieja, 2017;Valente et al, 2012;Yashina et al, 2019). Our results revealed that as the zebrafish develop from larval to juvenile stage, habenular circuits undergo multiple transitions in its architecture, sensory computations and intrinsically generated spontaneous activity, which could support the expansion of the behavioural repertoire in developing zebrafish.…”

“…In fact, a recent study revealed a sequential recruitment of neurons generating an increase in vHb activity, during the switch from active to passive coping behaviours in juvenile zebrafish (Andalman et al, 2019). Interestingly, such complex behaviours emerge at later stages of zebrafish development (Dreosti et al, 2015;Hinz and de Polavieja, 2017;Valente et al, 2012;Yashina et al, 2019), suggesting pronounced changes in the underlying circuitry across the brain. Despite extensive characterization of habenular circuitry during very early developmental stages (Aizawa et al, 2007;Bianco et al, 2008;deCarvalho et al, 2014), it is still unclear how the maturation of habenular networks and the establishment of its distinct functional modules corresponds to the observed expansion of animals behavioural repertoire during development.…”

The zebrafish dorsolateral habenula is required for updating learned behaviors

“…Series of recent studies highlight the increasing popularity of zebrafish for studying diverse aspects of animal behavior [30][31][32][33][34][35][36][37][38][39], including the more complex behaviors such as learning [25,26,[40][41][42][43][44][45][46] and social behaviors [47,48]. While studying complex behaviors in adult zebrafish allow investigation of brain function in a fully mature brain, larval and juvenile zebrafish has the tremendous advantage of a small and transparent brain, when it comes to studying brain A B C1 T1 C2 T2 T3 C3 T4 C4 T5 T6 control dHb activity [33,38,[49][50][51][52][53][54][55][56][57][58].…”

Molecular classification of zebrafish retinal ganglion cells links genes to cell types to behavior

“…Taken together, these results are consistent with a diversification model in which transcriptionally distinct immature RGCs in larvae are specified into adult RGC types in a gradual but possibly asynchronous fashion ( Figure 3I). This late diversification may underlie the post-larval emergence of visual behaviors such as shoaling and visual recognition of places, which are not observed until juvenile stages (Larsch and Baier, 2018;Yashina et al, 2019).…”