Focusing on optic tectum circuitry through the lens of genetics

Abstract

The visual pathway is tasked with processing incoming signals from the retina and converting this information into adaptive behavior. Recent studies of the larval zebrafish tectum have begun to clarify how the 'micro-circuitry' of this highly organized midbrain structure filters visual input, which arrives in the superficial layers and directs motor output through efferent projections from its deep layers. The new emphasis has been on the specific function of neuronal cell types, which can now be reproducibly labeled, imaged and manipulated using genetic and optical techniques. Here, we discuss recent advances and emerging experimental approaches for studying tectal circuits as models for visual processing and sensorimotor transformation by the vertebrate brain.

Figure 1

Classical and neoclassical methods of parsing the visual system. (a) Neural network underlying prey capture in anuran amphibians [3]. Anatomical studies from 1969 to 1999 were compiled to show the complex interconnectivity of visual and olfactory inputs, forebrain and midbrain contributions, and motor outputs. The retina is boxed in blue, and retinorecipient regions are boxed in red. Such schemes provide a framework for further study but do not address the pathways' micro-circuitry. A, anterior thalamus; PT, pretectum; OT, optic tectum; R, retina; V, ventral thalamus. Modified from [3]. (b) Scheme showing the major retinofugal connections in the larval zebrafish. Colored circles are stand-ins for diverse cell types, already known or yet to be discovered. The quantities in parentheses are estimates of the number of cell types (data compiled from work on zebrafish and other cyprinids). The retina comprises three cellular layers with five types of photoreceptors (4 cones, 1 rod), at least 11 bipolar cell types, about 70 amacrine cell types [100], and so on. The number of tectal neuron types is also large. Distinct RGC types (colors) likely have specific roles and connections with ten retinorecipient arborization fields (AF1 to AF9 plus AF10, which is the tectum) in the brain. Some anatomical details (as far as known): the RGCs that are connected to AF7 project a collateral to SO; RGC axons projecting to SAC/SPV in the tectum are routed through AF9. Abbreviations: AC, amacrine cell; AF, arborization field; BC, bipolar cell; GC, ganglion cell; HC, horizontal cell; INL, inner nuclear layer; IPL, inner plexiform layer; OPL, outer plexiform layer; PhR, photoreceptor; PVN, periventricular neuron; SAC, stratum album centrale; SFGS, stratum fibrosum et griseum superficiale; SGC, stratum griseum centrale; SIN, superficial interneuron; SO, stratum opticum; SPV, stratum periventriculare.

Figure 2

Cell type diversity and (some) functional connectivity of the fish optic tectum. (a) Cells described from classical Golgi studies in the adult goldfish tectum [19]. Fourteen types of neuron were identified on the basis of cell body position and morphology. Modified from [19]. (b) A sampling of neuron morphologies observed in the larval zebrafish tectum using 'genetic Golgi' methods. These include: radial glia (RG), periventricular projection neurons (PVPNs), periventricular interneurons (PVINs) and superficial interneurons (SINs). Retinorecipient laminae in the tectum are indicated by shading. Note the diverse dendrite morphologies of both projection neurons and interneurons in the tectum. In particular, PVINs have been observed containing arbors that are non-stratified (nsPVINs), mono-stratified (msPVINs) or bi-stratified (bsPVINs). (c) Hypothetical neural circuit responsible for size tuning of PVNs in the optic tectum [36]. Retinal afferents targeting the superficial layers of the SO and SFGS form excitatory synapses onto PVINs containing superficial dendrites and an axonal arbor in a deeper layer. These PVINs may mediate the vertical flow of excitation in response to small visual stimuli by activating PVPNs with dendrites located in deeper neuropil layers. In contrast, large visual stimuli additionally activate SIN cells, which inhibit the PVIN-mediated vertical flow of information to PVPNs.