Morphology, projection pattern, and neurochemical identity of Cajal's “centrifugal neurons”: The cells of origin of the tectoventrogeniculate pathway in pigeon (Columba livia) and chicken (Gallus gallus)

Abstract

The nucleus geniculatus lateralis pars ventralis (GLv) is a prominent retinal target in all amniotes. In birds, it is in receipt of a dense and topographically organized retinal projection. The GLv is also the target of substantial and topographically organized projections from the optic tectum and the visual wulst (Hyperpallium). Tectal and retinal afferents terminate homotopically within the external GLv-neuropil. Efferents from the GLv follow a descending course through the tegmentum, and can be traced into the medial pontine nucleus. At present, the cells of origin of the Tecto-GLv projection are only partially described. Here we have characterized the laminar location, morphology, projection pattern and neurochemical identity of these cells, by means of neural tracer injections and intracellular fillings in slice preparations and extracellular tracer injections in-vivo. The Tecto-GLv projection arises from a distinct subset of layer 10 bipolar neurons, whose apical dendrites show a complex transverse arborization at the level of layer 7. Axons of these bipolar cells arise from the apical dendrites and follow a course through the optic tract to finally form very fine and restricted terminal endings inside the GLv-neuropil. Double label experiments showed that these bipolar cells were ChAT immunoreactive. Our results strongly suggest that Tecto-GLv neurons form a pathway by which integrated tectal activity rapidly feeds back to the GLv and exerts a focal cholinergic modulation of incoming retinal inputs.

Microconnectomics of the pretectum and ventral thalamus in the chicken (Gallus gallus)

“…In the case of the TeO, GT‐collaterals ended in layer 13 probably onto SGC neurons (Fig. C,E), and in layer 10b possibly onto shepherd's crook (Sc) and/or vine neurons (Vega‐Zuniga et al, ) (Fig. D).…”

“…D). Regarding the role of these targeted cells, SGC neurons form part of the tectofugal pathway which has been linked to, e.g., luminance, color, motion, and looming (Wang et al, ); Sc neurons form part of the isthmo‐tectal loop involved in visual attention (Marín et al, ; Asadollahi et al, ), and vine neurons project back to the GLv (Vega‐Zuniga et al, ), which has been implicated in visuomotor control (Pateromichelakis, ; Guiloff et al, ). Furthermore, the GT is in receipt of direct retinal input (Gamlin and Cohen, ).…”

“…Finally, it is of interest to mention that the GLv‐TeO projection has been discussed since the 1980s. Several reports suggested the existence of a reciprocal topographic connection between both structures (Maturana and Varela, ; Guiloff et al, ), although it has been pointed out that the GLv‐TeO projection is not topographic and does not form a substantial organized connection as the TeO‐GLv (Vega‐Zuniga et al, ). This inconsistency might be due to differential injection depths used.…”

“…It is composed of two main layers: a lamina interna (li) that contains tightly packed somata, and a neuropil (ne) (Fig. ) with fewer cells that receives the retinal input (Crossland and Uchwat, ; Guiloff et al, ; Tömböl et al, ; Vega‐Zuniga et al, ). Previous studies have shown that the GLv projects to the area pretectalis (AP), LM (Hu et al, ), and presumably to the n. pontis medialis (PM) (Marín et al, ).…”

“…In birds, the pretectum and ventral thalamus contains several retino-recipient structures. Some of these nuclei, the n. lentiformis mesencephali (LM), the n. geniculatus lateralis pars ventralis (GLv), and the griseum tectale (GT), share a prominent retinotopy (Crossland and Uchwat, 1979;Gamlin and Cohen, 1988a;Vega-Zuniga et al, 2014). Numerous evidence indicates that these nuclei are connected directly and/or indirectly to neural structures involved in visuomotor control (du Lac and Knudsen, 1990;Masino and Knudsen, 1993;Wylie, 2001) and corollary discharges which may flow through axonal branches connecting imminent motor responses with sensory pathways (Crapse and Sommer, 2008;Yang et al, 2008).…”