Selective projection patterns from subtypes of retinal ganglion cells to tectum and pretectum: Distribution and relation to behavior

Abstract

An important issue to understand is how visual information can influence the motor system and affect behavior. Using the lamprey (Petromyzon marinus) as an experimental model we examined the morphological subtypes of retinal ganglion cells and their projection pattern to the tectum, which controls eye, head, and body movements, and to the pretectum, which mediates both visual escape responses and the dorsal light response. We identified six distinct morphological types of retinal ganglion cell. Four of these distribute their dendrites in the inner plexiform layer (image forming layer) and project in a retinotopic manner to all areas of the tectum. The posterior part of the retina has the highest density of ganglion cells and projects to the rostral part of the tectum, in which the visual field in front of the lamprey will be represented. From this area both orienting and evasive behaviors can be elicited. In contrast, pretectum receives input from two ganglion cells types that send their dendrites only to the outer plexiform layer or the outer limiting membrane and therefore may directly contact photoreceptors, and transmit information without additional delay to pretectum, which may be particularly important for visual escape responses. One of these two types, the bipolar ganglion cell, is only found in a small patch of retina just ventral of the optic nerve. Due to its distribution, morphology, and projections we suggest that this cell may control the dorsal light response.

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

“…To achieve this, we have developed a preparation in lamprey that maintains the eye and the midbrain intact in vitro, which has allowed us to perform whole-cell recordings from identified gaze-controlling cells in the optic tectum, while delivering natural and focal light stimuli within the visual field and monitoring and manipulating the synaptic responses. The retinotopic map in the lamprey tectum and the aligned motor map have been described in considerable detail (22,26), and the lamprey nervous system from forebrain to spinal cord is experimentally very accessible, well described, and also conserved throughout vertebrate evolution (30-32).Although most mammalian studies have focused on the role of the retinotopic excitatory circuits that mediate signal transmission between the superficial layer and the deeper layers (33-36), only more recent studies have emphasized the role of GABAergic circuits in the collicular control of gaze (37-45). The question how collicular GABAergic systems affect stimulus selection for gaze motor action has, however, remained unanswered because most studies have relied on extracellular recordings in vivo and therefore have not allowed an analysis of the synaptic basis for these inhibitory interactions.…”

“…To achieve this, we have developed a preparation in lamprey that maintains the eye and the midbrain intact in vitro, which has allowed us to perform whole-cell recordings from identified gaze-controlling cells in the optic tectum, while delivering natural and focal light stimuli within the visual field and monitoring and manipulating the synaptic responses. The retinotopic map in the lamprey tectum and the aligned motor map have been described in considerable detail (22,26), and the lamprey nervous system from forebrain to spinal cord is experimentally very accessible, well described, and also conserved throughout vertebrate evolution (30-32).…”

“…Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23)(24)(25)(26). The intermediate and deep layers give rise to projections to brainstem areas and a motor map is formed that is responsible for the coordination of eye, head, and body movements (22,(27)(28)(29).…”

Gating of steering signals through phasic modulation of reticulospinal neurons during locomotion

“…Visuomotor coordination (23) and steering results from activation of tectal output neurons that monosynaptically activate reticulospinal neurons (24,25), which represent the interface between tectum and the spinal cord networks. Here, we focus on the role of the phasic modulation of the reticulospinal neurons.…”

Neuronal organization of the brain in the adult amphioxus (Branchiostoma lanceolatum): A study with acetylated tubulin immunohistochemistry

“…Joseph cells, as with the Hesse ocellar cells, express amphioxus melanopsin and Gq and respond directly to light by depolarization (Koyanagi et al, 2005;Gomez et al, 2009) (Joseph cells) in the amphioxus brain is conceivably a pathway for the evolution of the vertebrate retina from a simple bilayered retina such as that observed in prolarvae of the sea lamprey (Mel endez-Ferro et al, 2002). This prolarval retina consists mainly of ciliary photoreceptors and ganglion cells that project to contralateral optic centers (de Miguel et al, 1990;Mel endez-Ferro et al, 2002), as most ganglion cells in large larvae and adults do (Vesselkin et al, 1980;de Miguel et al, 1990;Jones et al, 2009;Cornide-Petronio et al, 2011). Although the targets of Joseph cells were not assessed, Hesse photoreceptors exhibit contralateral projections (Castro et al, 2006), just as larval lamprey ganglion cells.…”