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A dedicated visual pathway for prey detection in larval zebrafish.

Semmelhack JL, Donovan JC, Thiele TR, Kuehn E, Laurell E, Baier H - Elife (2014)

Bottom Line: Two-photon calcium imaging revealed a small visual area, AF7, that was activated specifically by the optimal prey stimulus.We identified neurons with arbors in AF7 and found that they projected to multiple sensory and premotor areas: the optic tectum, the nucleus of the medial longitudinal fasciculus (nMLF) and the hindbrain.These findings indicate that computations in the retina give rise to a visual stream which transforms sensory information into a directed prey capture response.

View Article: PubMed Central - PubMed

Affiliation: Department Genes-Circuits-Behavior, Max Planck Institute of Neurobiology, Martinsried, Germany.

ABSTRACT
Zebrafish larvae show characteristic prey capture behavior in response to small moving objects. The neural mechanism used to recognize objects as prey remains largely unknown. We devised a machine learning behavior classification system to quantify hunting kinematics in semi-restrained animals exposed to a range of virtual stimuli. Two-photon calcium imaging revealed a small visual area, AF7, that was activated specifically by the optimal prey stimulus. This pretectal region is innervated by two types of retinal ganglion cells, which also send collaterals to the optic tectum. Laser ablation of AF7 markedly reduced prey capture behavior. We identified neurons with arbors in AF7 and found that they projected to multiple sensory and premotor areas: the optic tectum, the nucleus of the medial longitudinal fasciculus (nMLF) and the hindbrain. These findings indicate that computations in the retina give rise to a visual stream which transforms sensory information into a directed prey capture response.

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Model for prey capture circuitry.A prey stimulus on the left activates RGCs in the left eye (blue) which project to AF7 and the SO layer of the right tectum. Pretectal neurons (red) arborize in AF7 and send projections to the tectum or the nMLF and hindbrain. Activation of this circuitry produces a j-turn to the left, turning the larva in the direction of the prey. Previous studies have demonstrated connections between the tectum and nMLF (Gahtan et al., 2005) and between the tectum and hindbrain (Robles et al., 2011) (gray arrows).DOI:http://dx.doi.org/10.7554/eLife.04878.016
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fig8: Model for prey capture circuitry.A prey stimulus on the left activates RGCs in the left eye (blue) which project to AF7 and the SO layer of the right tectum. Pretectal neurons (red) arborize in AF7 and send projections to the tectum or the nMLF and hindbrain. Activation of this circuitry produces a j-turn to the left, turning the larva in the direction of the prey. Previous studies have demonstrated connections between the tectum and nMLF (Gahtan et al., 2005) and between the tectum and hindbrain (Robles et al., 2011) (gray arrows).DOI:http://dx.doi.org/10.7554/eLife.04878.016

Mentions: We have identified a class of pretectal neurons that have dendrites in the AF7 neuropil and also project to the most rostral fifth of the tectum (Figure 7A–C, Figure 7—figure supplement 1) which corresponds to the anterior visual field. If the motor map is roughly faithful to the visual map, tectal output neurons in this region could trigger prey capture forward swims. Within the pretectum, the AF7/tectum neurons also have processes in the non-retinorecipient neuropil next to AF7, which most likely corresponds to the magnocellular superficial pretectal nucleus (PSm). We hypothesize that these neurons could be integrating the retinal response to prey with information on behavioral state, and then providing excitatory input to the tectum when appropriate. These AF7 neurons project to a layer of the tectum just ventral to SO, the tectal layer that receives prey-responsive RGC axons (Figure 5B, Figure 8). Tectal neurons with dendrites in these superficial layers could thus receive positional information from the raw retinal input in the SO, and excitatory input from the AF7 neurons that would release prey capture behavior only under certain conditions. However, at this point we do not know the response properties or type of neurotransmitter released by these neurons, so we can only speculate as to the input they provide to the tectum.10.7554/eLife.04878.016Figure 8.Model for prey capture circuitry.


A dedicated visual pathway for prey detection in larval zebrafish.

Semmelhack JL, Donovan JC, Thiele TR, Kuehn E, Laurell E, Baier H - Elife (2014)

Model for prey capture circuitry.A prey stimulus on the left activates RGCs in the left eye (blue) which project to AF7 and the SO layer of the right tectum. Pretectal neurons (red) arborize in AF7 and send projections to the tectum or the nMLF and hindbrain. Activation of this circuitry produces a j-turn to the left, turning the larva in the direction of the prey. Previous studies have demonstrated connections between the tectum and nMLF (Gahtan et al., 2005) and between the tectum and hindbrain (Robles et al., 2011) (gray arrows).DOI:http://dx.doi.org/10.7554/eLife.04878.016
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Related In: Results  -  Collection

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fig8: Model for prey capture circuitry.A prey stimulus on the left activates RGCs in the left eye (blue) which project to AF7 and the SO layer of the right tectum. Pretectal neurons (red) arborize in AF7 and send projections to the tectum or the nMLF and hindbrain. Activation of this circuitry produces a j-turn to the left, turning the larva in the direction of the prey. Previous studies have demonstrated connections between the tectum and nMLF (Gahtan et al., 2005) and between the tectum and hindbrain (Robles et al., 2011) (gray arrows).DOI:http://dx.doi.org/10.7554/eLife.04878.016
Mentions: We have identified a class of pretectal neurons that have dendrites in the AF7 neuropil and also project to the most rostral fifth of the tectum (Figure 7A–C, Figure 7—figure supplement 1) which corresponds to the anterior visual field. If the motor map is roughly faithful to the visual map, tectal output neurons in this region could trigger prey capture forward swims. Within the pretectum, the AF7/tectum neurons also have processes in the non-retinorecipient neuropil next to AF7, which most likely corresponds to the magnocellular superficial pretectal nucleus (PSm). We hypothesize that these neurons could be integrating the retinal response to prey with information on behavioral state, and then providing excitatory input to the tectum when appropriate. These AF7 neurons project to a layer of the tectum just ventral to SO, the tectal layer that receives prey-responsive RGC axons (Figure 5B, Figure 8). Tectal neurons with dendrites in these superficial layers could thus receive positional information from the raw retinal input in the SO, and excitatory input from the AF7 neurons that would release prey capture behavior only under certain conditions. However, at this point we do not know the response properties or type of neurotransmitter released by these neurons, so we can only speculate as to the input they provide to the tectum.10.7554/eLife.04878.016Figure 8.Model for prey capture circuitry.

Bottom Line: Two-photon calcium imaging revealed a small visual area, AF7, that was activated specifically by the optimal prey stimulus.We identified neurons with arbors in AF7 and found that they projected to multiple sensory and premotor areas: the optic tectum, the nucleus of the medial longitudinal fasciculus (nMLF) and the hindbrain.These findings indicate that computations in the retina give rise to a visual stream which transforms sensory information into a directed prey capture response.

View Article: PubMed Central - PubMed

Affiliation: Department Genes-Circuits-Behavior, Max Planck Institute of Neurobiology, Martinsried, Germany.

ABSTRACT
Zebrafish larvae show characteristic prey capture behavior in response to small moving objects. The neural mechanism used to recognize objects as prey remains largely unknown. We devised a machine learning behavior classification system to quantify hunting kinematics in semi-restrained animals exposed to a range of virtual stimuli. Two-photon calcium imaging revealed a small visual area, AF7, that was activated specifically by the optimal prey stimulus. This pretectal region is innervated by two types of retinal ganglion cells, which also send collaterals to the optic tectum. Laser ablation of AF7 markedly reduced prey capture behavior. We identified neurons with arbors in AF7 and found that they projected to multiple sensory and premotor areas: the optic tectum, the nucleus of the medial longitudinal fasciculus (nMLF) and the hindbrain. These findings indicate that computations in the retina give rise to a visual stream which transforms sensory information into a directed prey capture response.

Show MeSH
Related in: MedlinePlus