Sustained Rhythmic Brain Activity Underlies Visual Motion Perception in Zebrafish (original) (raw)

Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion

eLife, 2016

In the absence of salient sensory cues to guide behavior, animals must still execute sequences of motor actions in order to forage and explore. How such successive motor actions are coordinated to form global locomotion trajectories is unknown. We mapped the structure of larval zebrafish swim trajectories in homogeneous environments and found that trajectories were characterized by alternating sequences of repeated turns to the left and to the right. Using wholebrain light-sheet imaging, we identified activity relating to the behavior in specific neural populations that we termed the anterior rhombencephalic turning region (ARTR). ARTR perturbations biased swim direction and reduced the dependence of turn direction on turn history, indicating that the ARTR is part of a network generating the temporal correlations in turn direction. We also find suggestive evidence for ARTR mutual inhibition and ARTR projections to premotor neurons. Finally, simulations suggest the observed turn sequences may underlie efficient exploration of local environments.

Year : 2009 Illusionary self-motion perception in zebrafish

2009

Zebrafish mutant belladonna (bel) carries a mutation in the lhx2 gene (encoding a Lim domain homeobox transcription factor) that results in a defect in retinotectal axon pathfinding, which can lead to uncrossed optic nerves failing to form an optic chiasm. Here, we report on a novel swimming behavior of the bel mutants, best described as looping. Together with two previously reported oculomotor instabilities that have been related to achiasmatic bel mutants, reversed optokinetic response (OKR) and congenital nystagmus (CN, involuntary conjugate oscillations of both eyes), looping opens a door to study the influence of visual input and eye movements on postural balance. Our result shows that looping correlates perfectly with reversed OKR and CN and is vision-dependent and contrast sensitive. CN precedes looping and the direction of the CN slow phase is predictive of the looping direction, but is absent during looping. Therefore, looping may be triggered by CN in bel. Moreover, loopin...

Sensorimotor computation underlying phototaxis in zebrafish

Nature Communications, 2017

Animals continuously gather sensory cues to move towards favourable environments. Efficient goal-directed navigation requires sensory perception and motor commands to be intertwined in a feedback loop, yet the neural substrate underlying this sensorimotor task in the vertebrate brain remains elusive. Here, we combine virtual-reality behavioural assays, volumetric calcium imaging, optogenetic stimulation and circuit modelling to reveal the neural mechanisms through which a zebrafish performs phototaxis, i.e. actively orients towards a light source. Key to this process is a self-oscillating hindbrain population (HBO) that acts as a pacemaker for ocular saccades and controls the orientation of successive swim-bouts. It further integrates visual stimuli in a state-dependent manner, i.e. its response to visual inputs varies with the motor context, a mechanism that manifests itself in the phase-locked entrainment of the HBO by periodic stimuli. A rate model is developed that reproduces ou...

Illusionary Self-Motion Perception in Zebrafish

PLoS ONE, 2009

Neural Control and Modulation of Swimming Speed in the Larval Zebrafish

2014

Vertebrate locomotion at different speeds is driven by descending excitatory connections to central pattern generators in the spinal cord. To investigate how these inputs determine locomotor kinematics, we used whole-field visual motion to drive zebrafish to swim at different speeds. Larvae match the stimulus speed by utilizing more locomotor events, or modifying kinematic parameters such as the duration and speed of swimming bouts, the tail-beat frequency, and the choice of gait. We used laser ablations, electrical stimulation, and activity recordings in descending neurons of the nucleus of the medial longitudinal fasciculus (nMLF) to dissect their contribution to controlling forward movement. We found that the activity of single identified neurons within the nMLF is correlated with locomotor kinematics, and modulates both the duration and oscillation frequency of tail movements. By identifying the contribution of individual supraspinal circuit elements to locomotion kinematics, we build a better understanding of how the brain controls movement.

Spatiotemporal Transition in the Role of Synaptic Inhibition to the Tail Beat Rhythm of Developing Larval Zebrafish

eneuro, 2020

Significant maturation of swimming in zebrafish (Danio rerio) occurs within the first few days of life when fish transition from coiling movements to burst swimming and then to beat-and-glide swimming. This maturation occurs against a backdrop of numerous developmental changes-neurogenesis, a transition from predominantly electrical to chemical-based neurotransmission, and refinement of intrinsic properties. There is evidence that spinal locomotor circuits undergo fundamental changes as the zebrafish transitions from burst to beat-and-glide swimming. Our electrophysiological recordings confirm that the operation of spinal locomotor circuits becomes increasingly reliant on glycinergic neurotransmission for rhythmogenesis governing the rhythm of tail beats. This

Visual motion induces synchronous oscillations in turtle visual cortex

Proceedings of the National Academy of Sciences of the United States of America, 1994

In mammalian brains, multielectrode recordings during sensory stimulation have revealed oscillations in different cortical areas that are transiently synchronous. These synchronizations have been hypothesized to support integration of sensory information or represent the operation of attentional mechanisms, but their stimulus requirements and prevalence are still unclear. Here I report an analogous synchronization in a reptilian cortex induced by moving visual stimuli. The synchronization, as measured by the coherence function, applies to spindle-like 20-Hz oscillations recorded with multiple electrodes implanted in the dorsal cortex and the dorsal ventricular ridge of the pond turtle. Additionally, widespread increases in coherence are observed in the 1to 2-Hz band, and widespread decreases in coherence are seen in the 10-and 30to 45-Hz bands. The 20-Hz oscillations induced by the moving bar or more natural stimuli are nonstationary and can be sustained for seconds. Early reptile studies may have interpreted similar spindles as electroencephalogram correlates of arousal; however, the absence of these spindles during arousing stimuli in the dark suggests a more specific role in visual processing. Thus, visually induced synchronous oscillations are not unique to the mammalian cortex but also occur in the visual area of the primitive three-layered cortex of reptiles.

Representation of Border, Velocity and Speed in the Goldfish Brain

bioRxiv (Cold Spring Harbor Laboratory), 2018

Like most animals, the survival of fish depends on navigation in space. This capacity has been documented in behavioral studies that have revealed navigation strategies. However, little is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. We found that cells in the lateral pallium of the goldfish encode the edges of the environment, the fish head direction, the fish swimming speed, and the fish swimming velocity-vector. This study sheds light on how information related to navigation is represented in the brain of fish and addresses the fundamental question of the neural basis of navigation in this group of vertebrates. Navigation is a fundamental behavioral capacity facilitating survival in many animal species 1-4. It involves the continuous estimation and representation of the animal's position and direction in the environment, which are implemented in the planning and execution of movements and trajectories towards target locations 5,6. Navigation has been extensively investigated in numerous taxa across the animal kingdom, but attempts to probe its neural substrate have mainly been focused on mammals 7 and insects 8. In mammals, neurons in the hippocampal formation encode information about the position and orientation of the animal in space 5-7,9,10. These cells include place cells 11 , grid cells 12 , head direction cells 13,14 , and other cell types 15,16. In insects, a ring-shaped neural network in the central complex of the fruit fly was shown to represent its heading direction 8. Teleost fish, which form the largest vertebrate class, have shown to have many high cognitive abilities with navigation among them 17-23. To better understand space representation in non-mammalian vertebrates, we explored the neural substrate of navigation in the goldfish (Carassius auratus) as a representative of the teleost class. These fish are known to be able to navigate by exploiting either an allocentric or an egocentric frame of reference 24. This may imply that the goldfish has the ability to build an internal representation of space in the form of a cognitive map 25. This would include cognitive map-like navigation strategies to find a goal when starting from an unfamiliar initial position or taking shorter alternative routes (shortcuts) when possible 25-28. Furthermore, goldfish integrate many environmental cues when navigating 29-31 ; therefore, a change of a single cue does not impair their navigation ability in known environment 27,29. Previous work by Canfield and Mizumori describe a method for extracellular recording system in tethered goldfish. Their paper provides preliminary evidence for speed and spatial encoding in the goldfish lateral pallium 32. In addition, lesion studies in goldfish have shown that the fish pallium, which is the dorsal part of the telencephalon, is crucial for spatial navigation. A lesion in the lateral areas of the pallium leads to impairment in allocentric spatial memory and learning, but not when the lesion affects other parts of the telencephalon 27. These findings are similar to results from lesions studies of the hippocampus in mammals and further strengthen the

Representation of Borders and Swimming Kinematics in the Brain of Freely-Navigating Fish

2018

Like most animals, the survival of fish depends crucially on navigation in space. This capacity has been documented in numerous behavioral studies that have revealed navigation strategies and the sensory modalities used for navigation. However, virtually nothing is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a novel wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. Four cell types were identified: border cells, head direction cells, speed cells and conjunction head direction with speed. Border cells were active when the fish was near the boundary of the environment. Head direction cells were shown to encode head direction. Speed cells only encoded the absolute speed independent of direction suggestive of an odometry signa...

Sustained Rhythmic Brain Activity Underlies Visual Motion Perception in Zebrafish (original) (raw)

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