Brain-wide neuronal dynamics during motor adaptation in zebrafish

Ahrens, Misha B.; Li, Jennifer M.; Orger, Michael B.; Robson, Drew N.; Schier, Alexander F.; Engert, Florian; Portugues, Rubén

doi:10.1038/nature11057

Cited by 645 publications

(677 citation statements)

References 52 publications

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“…The Drosophila larva is likely to be the next animal, after C. elegans, that offers a complete wiring diagram of an entire nervous system with synaptic resolution (41). Advances in optical neurophysiology may soon make it possible to record the activities of large ensembles of neurons in the Drosophila larva, as has recently been accomplished in C. elegans and zebrafish larva (42)(43)(44)(45).…”

Section: Discussionmentioning

confidence: 99%

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Klein

Afonso

Vonner

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

152

206

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Complex animal behaviors are built from dynamical relationships between sensory inputs, neuronal activity, and motor outputs in patterns with strategic value. Connecting these patterns illuminates how nervous systems compute behavior. Here, we study Drosophila larva navigation up temperature gradients toward preferred temperatures (positive thermotaxis). By tracking the movements of animals responding to fixed spatial temperature gradients or random temperature fluctuations, we calculate the sensitivity and dynamics of the conversion of thermosensory inputs into motor responses. We discover three thermosensory neurons in each dorsal organ ganglion (DOG) that are required for positive thermotaxis. Random optogenetic stimulation of the DOG thermosensory neurons evokes behavioral patterns that mimic the response to temperature variations. In vivo calcium and voltage imaging reveals that the DOG thermosensory neurons exhibit activity patterns with sensitivity and dynamics matched to the behavioral response. Temporal processing of temperature variations carried out by the DOG thermosensory neurons emerges in distinct motor responses during thermotaxis. N avigation toward environmental conditions that improve survival and fitness is of near-universal importance in motile biological organisms. Quantitative analysis of such animal behaviors to defined sensory inputs is a powerful approach to elucidate how behavior is encoded in underlying neurons and circuits. The advantage of studying navigation in small, optically transparent, genetically modifiable animals like Caenorhabditis elegans (1) or Drosophila larvae (2) is the opportunity to dissect sensory, neuronal, and behavioral dynamics in live animals by using optical neurophysiology and optogenetics throughout the nervous system.The Drosophila melanogaster larva navigates gradients of many sensory cues, including light, temperature, odors, and tastes, but with fewer neurons in its sensory periphery and brain than the adult. Moreover, the simpler body plan and crawling movements of the larva facilitate the precise quantification of behavioral dynamics. Poikilotherms like C. elegans or Drosophila use sensitive thermosensory mechanisms to navigate moderate temperature ranges, thereby enabling them to use their environments to regulate their own body temperatures (3, 4). Here, we study sensory and behavioral dynamics during positive thermotaxis (i.e., cool avoidance) by the Drosophila larva. Tracking the movements of Drosophila exploring temperature, olfactory, or gaseous gradients has shown that their navigation is generated by a sequence of two alternating motor programs: runs involving peristaltic forward movement that are interrupted by turns involving probing side-to-side head sweeps until the initiation of a new run (5-8). Larvae negotiating temperature gradients stochastically transition between runs and turns by strategies that cause runs pointed in favorable directions to be more frequent and longer than runs pointed in unfavorable directions. These transitions b...

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Section: Discussionmentioning

confidence: 99%

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Klein

Afonso

Vonner

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

152

206

View full text Add to dashboard Cite

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“…One solution is to provide a virtual reality environment such that the visual feedback the fish receives indicates it is moving (i.e. fictive movement) [67,68]. Another approach that allows the fish to slightly 'move' in a way that does not disturb brain imaging is to permit tail movement, while the remaining body, especially the head, is embedded in agarose.…”

Section: (B) Virtual Environment and Conditioned Tail Movementmentioning

confidence: 99%

Zebrafish forebrain and temporal conditioning

Cheng

Jesuthasan

Penney

2014

Phil. Trans. R. Soc. B

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The rise of zebrafish as a neuroscience research model organism, in conjunction with recent progress in single-cell resolution whole-brain imaging of larval zebrafish, opens a new window of opportunity for research on interval timing. In this article, we review zebrafish neuroanatomy and neuromodulatory systems, with particular focus on identifying homologies between the zebrafish forebrain and the mammalian forebrain. The neuroanatomical and neurochemical basis of interval timing is summarized with emphasis on the potential of using zebrafish to reveal the neural circuits for interval timing. The behavioural repertoire of larval zebrafish is reviewed and we demonstrate that larval zebrafish are capable of expecting a stimulus at a precise time point with minimal training. In conclusion, we propose that interval timing research using zebrafish and whole-brain calcium imaging at single-cell resolution will contribute to our understanding of how timing and time perception originate in the vertebrate brain from the level of single cells to circuits.

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“…For example, to accurately sense the external world while simultaneously moving within it, the nervous system must be able to detect changes in its sensory inputs that are not a predictable consequence of self-motion. Indeed, many sensory neurons respond with high sensitivity to unpredictable stimuli during motor behavior despite self-caused sensory feedback (1)(2)(3)(4)(5). Such remarkable sensitivity can be achieved by circuit mechanisms that counteract sensory feedback associated with self-generated motor output (6).…”

mentioning

confidence: 99%

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

Giret

Kornfeld²,

Ganguli

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Learning by imitation is fundamental to both communication and social behavior and requires the conversion of complex, nonlinear sensory codes for perception into similarly complex motor codes for generating action. To understand the neural substrates underlying this conversion, we study sensorimotor transformations in songbird cortical output neurons of a basal-ganglia pathway involved in song learning. Despite the complexity of sensory and motor codes, we find a simple, temporally specific, causal correspondence between them. Sensory neural responses to song playback mirror motor-related activity recorded during singing, with a temporal offset of roughly 40 ms, in agreement with short feedback loop delays estimated using electrical and auditory stimulation. Such matching of mirroring offsets and loop delays is consistent with a recent Hebbian theory of motor learning and suggests that cortico-basal ganglia pathways could support motor control via causal inverse models that can invert the rich correspondence between motor exploration and sensory feedback.lateral magnocellular nucleus of the anterior nidopallium | Hebbian learning | mirror neuron

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Brain-wide neuronal dynamics during motor adaptation in zebrafish

Cited by 645 publications

References 52 publications

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Zebrafish forebrain and temporal conditioning

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

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