The Serotonergic System Tracks the Outcomes of Actions to Mediate Short-Term Motor Learning

Kawashima, Takashi; Zwart, Maarten; Yang, Chao-Tsung; Mensh, Brett D.; Ahrens, Misha B.

doi:10.1016/j.cell.2016.09.055

Cited by 126 publications

(149 citation statements)

References 63 publications

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“…This proposal also finds support in a recent study showing that DRN 5-HT activity mediates short-term sensorimotor adaptation in zebrafish, by reporting the difference between the expected and actual sensory consequences of motor commands (Kawashima et al, 2016). However, further experiments will clearly be necessary to test these ideas as explanations of the present data.…”

Section: Discussionsupporting

confidence: 70%

Activity patterns of serotonin neurons underlying cognitive flexibility

Matias¹,

Lottem

Dugué

et al. 2017

eLife

213

222

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Serotonin is implicated in mood and affective disorders. However, growing evidence suggests that a core endogenous role is to promote flexible adaptation to changes in the causal structure of the environment, through behavioral inhibition and enhanced plasticity. We used long-term photometric recordings in mice to study a population of dorsal raphe serotonin neurons, whose activity we could link to normal reversal learning using pharmacogenetics. We found that these neurons are activated by both positive and negative prediction errors, and thus report signals similar to those proposed to promote learning in conditions of uncertainty. Furthermore, by comparing the cue responses of serotonin and dopamine neurons, we found differences in learning rates that could explain the importance of serotonin in inhibiting perseverative responding. Our findings show how the activity patterns of serotonin neurons support a role in cognitive flexibility, and suggest a revised model of dopamine–serotonin opponency with potential clinical implications.DOI: http://dx.doi.org/10.7554/eLife.20552.001

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Section: Discussionsupporting

confidence: 70%

Activity patterns of serotonin neurons underlying cognitive flexibility

Matias¹,

Lottem

Dugué

et al. 2017

eLife

213

222

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“…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]. Hence, we investigated the ontogeny of a complex operant behavior, namely CPA learning, and showed that the learning performance of young zebrafish improves across development.…”

Section: Discussionmentioning

confidence: 99%

The zebrafish dorsolateral habenula is required for updating learned behaviors

Palumbo

Serneels

Pelgrims

et al. 2019

Preprint

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Operant conditioning requires multiple cognitive processes, such as learning, consolidation, prediction of potential outcomes and decision making. It is less clear how interactions of these processes led to behavioral adaptations that allows animal to cope with changing environment. We first showed that juvenile zebrafish can perform conditioned place avoidance learning, with improving performance across development. Next, we disentangled operant conditioning from contextual fear and anxiety. Our results revealed that animals' decisions and learning performance is shaped by the available information and animals' experience. Ablation of dorsal habenula (dHb), a brain region involved in learning and prediction of outcomes, led to an unexpected improvement in animals learning performance and delayed memory extinction. Interestingly, while the control animals' exhibit rapid adaptation to changing learning rules, dHb ablated animals failed to adapt. Altogether, our results showed that dHb plays a central role in switching animals' strategies while integrating new evidences with prior experience. Eggen, M. Andresen, V. Nguyen, A Nygard and our fish facility support team for technical assistance. We thank Nathalie Jurisch-Yaksi and Stephanie Fore for helpful comments on the text. We thank all Yaksi lab members for stimulating discussions. This work was funded by ERC starting grant 335561 (F.P., R.P., E.Y.) and RCN FRIPRO Research Grant 239973 (E.Y.). Work in the E.Y. lab is funded by the Kavli Institute for Systems Neuroscience at NTNU. AUTHOR CONTRIBUTIONSConceptualization, F.P., E.Y.; Methodology and data, F.P., B.S.; Recording software F.P., R.P.; Data

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“…The larval zebrafish is an ideal vertebrate model for the detailed study of behaviour and its associated circuits. They have a diverse behavioural repertoire that can be precisely measured [31,41], and neural activity can be recorded non-invasively and at single-neuron resolution throughout the whole brain [1,29,40,45,57]. Larval hunting appears as a distinct behavioural mode that is composed of several component actions chained together into a sequence [9,33,51].…”

Section: Introductionmentioning

confidence: 99%

Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae

Lagogiannis

Diana

Meyer

2019

Preprint

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The success of goal-directed behaviours relies on the coordinated execution of a sequence of component actions. In young animals, such sequences may be poorly coordinated, but with age and experience, behaviour progressively adapts to efficiently exploit the animal's ecological niche. How experience impinges on the developing neural circuits of behaviour is an open question. As a model system, larval zebrafish (Danio rerio) hold enormous potential for studying both the development of behaviour and the underlying circuits, but no relevant experience-dependent learning paradigm has yet been characterized. To address this, we have conducted a detailed study of the effects of experience on the ontogeny of hunting behaviour in larval zebrafish. We report that larvae with prior prey experience consume considerably more prey than naive larvae. This is mainly due to increased capture success that is also accompanied by a modest increase in hunt rate. We identified two components of the hunting sequence that are jointly modified by experience. At the onset of the hunting sequence, the orientation strategy of the turn towards prey is modified such that experienced larvae undershoot prey azimuth. Near the end of the hunt sequence, we find that experienced larvae are more likely to employ high-speed capture swims initiated from longer distances to prey. Combined, these modified turn and capture manoeuvrers can be used to predict the probability of capture success and suggest that their development provides advantages specific to larvae feeding on live-prey. Our findings establish an ethologically relevant paradigm in zebrafish for studying how the brain is shaped by experience to drive the ontogeny of efficient behaviour.

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The Serotonergic System Tracks the Outcomes of Actions to Mediate Short-Term Motor Learning

Cited by 126 publications

References 63 publications

Activity patterns of serotonin neurons underlying cognitive flexibility

Activity patterns of serotonin neurons underlying cognitive flexibility

The zebrafish dorsolateral habenula is required for updating learned behaviors

Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae

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