Retinofugal Projections
Retinal ganglion cells transmit visual information from the retina to the brain. 10 arborisation fields (AF) or retino-recipient brain areas have been identified in zebrafish (Burrill & Easter., 2004). 97% of retinal ganglion cell(RGC) axons terminate in the optic tectum (Arborisation field AF-10), with the remaining 3% terminating in AF-9. The other 9 arborisation fields are innervated by RGC axon collaterals. Single RGC axons can innervate multiple AFs before terminating in the optic tectum. Each AF in the larvae corresponds to a retino-recipient nucleus in the adult diencephalon (Robles et al., 2014). The visual system and how different types of visual stimuli affect behaviour is a very popular field of research in zebrafish. For an overview of connectivity and function of each AF and possible adult identities of these retino-recipient nuclei please read the individual tutorials.
Schematic showing the locations of the 10 arborisation fields in a 6dpf zebrafish. The optic tract is labelled in the Tg(atoh7:RFP) transgenic line and position of AFs are based on the data from Robles (2014).
Transverse 3D section of atoh7:gapRFP reference brain showing most retinal arborisation fields (AF2–10). In the right hemisphere, RFP has been pseudo-coloured to demarcate specific AFs. Adapted from data in Antinucci et al., 2019.
A flythrough movie of a registered elavl3:H2B-GCaMP6s;atoh7:gapRFP larvae with the AFs pseudo-coloured can be seen here as part of the supplementary data for Antinucci et al(2019).
Click on a tutorial below to read more about the neuroanatomy and function of each AF.
some Arborisation fields receive biased retinal input
Schematics showing the result of DiI and DiD injections into dorsal and ventral hemiretinas of the contralateral eye.
DiI and DiD injections into dorsal and ventral retina. Schematic adapted from Robles et al 2014.
AF-6 is innervated more by RGCs in the dorsal retina.
Schematic created based on data in Robles 2014.
AF-1, AF-4 and AF-8 are innervated more by RGCs located in ventral retina.
Schematic created based on data in Robles 2014.
Schematics showing the result of DiI and DiD injections into nasal and temporal hemiretinas of the contralateral eye.
DiI and DiD injections into nasal and temporal retina. Schematic adapted from Robles et al 2014.
AF-7 shows preferential innervation by RGCs located in nasal retina. All other AFs receive broadly equal innervation by nasal and temporally located RGCs.
Schematic created based on data in Robles 2014.
Visual behaviours in larval zebrafish
Different arborisation fields are associated with different visual behaviours. Check the individual tutorials for each AF to see which visual behaviours each AF is associated with.
Prey capture in zebrafish is a visually guided behaviour. Zebrafish larvae exhibit specific motor (J-turns and pectoral fin movements) and oculomotor responses (eye convergence) in response to prey-like stimuli. 2-photon calcium imaging of tethered zebrafish larval brain presented with virtual prey-like stimuli have identified AF-7 (Semmelhack et al., 2014) and clusters of tectal neurons (AF-10) that are selective for prey-like moving spots (Del Bene et al., 2010; Bianco & Engert., 2015).
The optomotor response (OMR): fish will swim to stabilise their position with respect to a drifting visual background. When a zebrafish larvae is presented with a whole-field motion stimulus, such as a forward-moving binary grating, the fish will swim in the direction of the perceived motion. (Kist & Portugues., 2019; Kubo., 2014; Orger et al., 2008).
A highly conserved innate behaviour. Larval zebrafish placed in a light-dark choice assay show a significant preference towards light. This light-preference behaviour is mediated by the habenula. The presence and intensity of ambient light is encoded in light responsive habenula neurons that receive input from prethalamic neurons that arborise with ventrally located RGCs at AF-4 (Zhang et al., 2017; Cheng et al.,2017).
The optokinetic response (OKR) is an eye tracking movement where objects moving across the visual field evoke stereotyped eye movements. These saccades are composed of two parts: a smooth pursuit of the object followed by a quick saccade in the opposit direction to reset the eyes once the stimulus has left the visual field. The OKR and the optomotor response (OMR) are both examples of gaze-stabilising behaviours in which the eyes move to hold the gaze steady (Kramer et al., 2019).
A Looming stimulus is representative of an object on a collision course with the larvae. This type of object could represent either an obstacle or a predator. In an experimental context this type of stimulus can be represented in 2D by an expanding disk. Looming stimuli elicit stereotyped innate responses such as freezing of escape responses. In zebrafish tethered larvae presented with looming stimuli perform escape swims composed of a C-bend curvature of the tail followed by a fast forward swim. The C-bend turns the larvae away from the looming stimulus while the fast forward swim propels the larvae away. AF-6, AF-8 and the optic tectum AF-10 have been shown using 2-photon calcium imaging to be activated by looming stimuli (Temizer et al., 2015).
Larval zebrafish exhibit a circular swimming behaviour immediately following a loss of illumination. Individual larvae show a left/right directional bias in this behaviour, and will mostly circle in the same direction. The direction of turning preference is stochastic within the population. Horstick et al identified a group of neurons in the anterior part of the posterior tuberculum(PT) that are proximal to AF3 whose firing pattern that correlates well with the initiation and duration of this darkness-induced circling behaviour. These PT neurons project to the ipsilateral habenula. This PT-habenula pathway imposes left/right biases on motor responses (Horstick et al.2020).
Publications
Robles, E., Laurell, E., Baier, H. (2014)
The Retinal Projectome Reveals Brain-Area-Specific Visual Representations Generated by Ganglion Cell Diversity.
Current biology : CB. 24(18):2085-96.
Burrill JD & Easter Jr SS
Development of the Retinofugal projections.
J Comp Neurology, 2004 pp.1-18.
Semmelhack, J.L., Donovan, J.C., Thiele, T.R., Kuehn, E., Laurell, E., Baier, H. (2014)
A dedicated visual pathway for prey detection in larval zebrafish.
eLIFE. 4:299-307.
Orger, M.B., Kampff, A.R., Severi, K.E., Bollmann, J.H., and Engert, F. (2008)
Control of visually guided behavior by distinct populations of spinal projection neurons.
Nature Neuroscience. 11(3):327-333.
Orger, M.B. (2016)
The Cellular Organization of Zebrafish Visuomotor Circuits.
Current biology : CB. 26:R377-R385.
Bianco & Engert (2015)
Visuomotor Transformations Underlying Hunting Behavior in Zebrafish
Current Biology, 25 (2015) 831-846. doi:10.1016/j.cub.2015.01.042
Kist AM & Portugues R (2019)
Optomotor Swimming in Larval Zebrafish Is Driven by Global Whole-Field Visual Motion and Local Light- Dark Transitions.
Cell Reports, 29 659-673.
Antinucci P, Folgueira M, Bianco IH.
Pretectal neurons control hunting behaviour.
eLife (2019) 8 doi.org/10.7554/eLife.48114
Temizer, I. et al (2015)
A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish.
Current Biology, 25(14), pp.1823–1834.
Kramer, A., Wu, Y., Baier, H., Kubo, F. (2019)
Neuronal Architecture of a Visual Center that Processes Optic Flow.
Neuron. 103(1):118-132.e7.
Del Bene, F., Wyart, C., Robles, E., Tran, A., Looger, L., Scott, E.K., Isacoff, E.Y., and Baier, H. (2010)
Filtering of visual information in the tectum by an identified neural circuit.
Science (New York, N.Y.). 330(6004):669-673.
Romano, S.A., Pietri, T., Pérez-Schuster, V., Jouary, A., Haudrechy, M., Sumbre, G. (2015)
Spontaneous Neuronal Network Dynamics Reveal Circuit's Functional Adaptations for Behavior.
Neuron. 85(5):1070-85.
Gebhardt C, Auer TO, Henriques PM, Rajan G, Duroure K, Bianco IH*, Del Bene F*.
An interhemispheric neural circuit allowing binocular integration in the optic tectum.
Nature Communications (2019) 10, 5471. doi:10.1038/s41467-019-13484-9
Zhang, B.B., Yao, Y.Y., Zhang, H.F., Kawakami, K., Du, J.L. (2017)
Left Habenula Mediates Light-Preference Behavior in Zebrafish via an Asymmetrical Visual Pathway.
Neuron. 93(4):914-928.e4.
Cheng, R.K., Krishnan, S., Lin, Q., Kibat, C., Jesuthasan, S. (2017)
Characterization of a thalamic nucleus mediating habenula responses to changes in ambient illumination.
BMC Biology. 15:104.
Heap, L.A.L., Vanwalleghem, G., Thompson, A.W., Favre-Bulle, I.A., Scott, E.K. (2018)
Luminance Changes Drive Directional Startle through a Thalamic Pathway.
Neuron. 99(2):293-301.e4.
Förster, D., Helmbrecht, T.O., Mearns, D.S., Jordan, L., Mokayes, N., Baier, H. (2020)
Retinotectal circuitry of larval zebrafish is adapted to detection and pursuit of prey.
eLIFE. 9:e58596. DOI: https://doi.org/10.7554/eLife.58596