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. J. Comp. Neurol. 517:257–275, 2009. © 2009 Wiley‐Liss, Inc.

The evolutionary origin of visual and somatosensory representation in the vertebrate pallium

“…This suggests an overall maintenance of hardwired retinotopic specificity both in thalamus and the visual cortex (Extended Data Fig. 5) in addition to the optic tectum 43 , similar to what has been described in mammals 44,45 . The thalamic projection neurons to the visual and somatosensory areas are distinct and separate from those projecting to striatum (Extended Data Fig.…”

“…The retinotopic specificity is also present at the level of thalamus and as shown earlier in the optic tectum 43 . It would seem that sensory channels and specificity like retinotopy and somatotopy evolved as a common design of sensorimotor processing very early in vertebrate evolution (see Fig.…”

“…With respect to specificity, the retinotopy is also present at the level of thalamus with visual thalamocortical neurons receiving retinal input from distinct parts of the optic tract. This implies that the retinotopic organisation is an inherent feature of visual processing at three different levels in the lamprey brain, namely cortex and thalamus in addition to the optic tectum 43 . The somatosensory information from the dorsal column and the trigeminal afferents are relayed to thalamus through the lemniscal pathways via the dorsal column nucleus and the trigeminal sensory nucleus, respectively.…”

Resynthesizing behavior through phylogenetic refinement

“…Microstimulation has also revealed a region in the rostral part of the lamprey tectum that produces behavior orienting toward objects—including eye and head turning followed by swimming. Interestingly, this region of the tectum receives input from a part of the retina that is sensitive to space in front of the animal with a complex collection of retinal ganglion cells, and it projects mostly contra laterally to the spinal cord (Jones, Grillner, & Robertson, 2009; Kardamakis, Saitoh, & Grillner, 2015). In short, it implements approach behavior (Fig.…”

The neural bases of vertebrate motor behaviour through the lens of evolution

“…The eye motor nuclei (III, IV and VI) are organized similarly [16], as well as the trigeminal nerve (nerve V). The optic nerve (nerve II) projects to the thalamus and the superior colliculus and provides a retinotopic representation in both structures [13,17,18]. The olfactory input (nerve I) is organized with olfactory receptor cells projecting to separate glomeruli [19,20], and the information is carried further via two separate avenues-the mitral and the tufted olfactory projection neurons in both groups [21] (figure 3).…”