Pretectal and tectal afferents to the dorsal lateral geniculate nucleus of the turtle: An electron microscopic axon tracing and γ‐aminobutyric acid immunocytochemical study

Abstract

The pretectal and tectal projections to the dorsal lateral geniculate nucleus (GLd) of two species of turtle (Emys orbicularis and Testudo horsfieldi) were examined under the electron microscope by using axonal tracing techniques (horseradish peroxidase or biotinylated dextran amine) and postembedding gamma-aminobutyric acid (GABA) immunocytochemistry. After injection of tracer into the pretectum, two types of axon terminals were identified as those of pretectogeniculate pathways. Both contained pleomorphic synaptic vesicles and were more numerous in the inner part of the nucleus. They could be distinguished on the bases of size and shape of their synaptic vesicles, type of synaptic contact, and level of GABA immunoreactivity. One type had a higher density of immunolabeling and established symmetric synaptic contacts, whereas the other, less densely immunolabeled, made asymmetric synaptic contacts. In both cases, synaptic contacts were mainly with relay cells and occasionally with interneurons. We suggest that these two types of pretectogeniculate terminals originate in two separate pretectal nuclei. After injection of tracer into the optic tectum, a single population of GABA-immunonegative tracer-labeled terminals was identified as belonging to the tectogeniculate pathway. These were small, had smooth contours, contained very small round synaptic vesicles, and established asymmetric synaptic contacts with long active zones, predominantly with relay cells and less frequently with interneurons, in the inner part of the nucleus. In addition, a population of GABA-negative and occasionally GABA-positive terminals, labeled by tracer injected into either the pretectum or the tectum, was identified as retinal terminals; these were presumably labeled by the retrograde transport of tracer in collateral branches of visual fibers innervating both the GLd and the pretectum or tectum. Comparison of the present ultrastructural findings in turtles with those previously reported in mammals shows that the cytological features, synaptic morphology, and immunochemical properties of the pretectogeniculate and tectogeniculate terminals of both groups share many similarities. Nevertheless, the postsynaptic targets of these two categories of terminals display some pronounced differences between the two groups, which are discussed in terms of their possible functional significance.

Fine structure of the visual dorsolateral anterior thalamic nucleus of the pigeon (Columba livia): A hodological and GABA‐immunocytochemical study

“…In reptiles an entirely comparable GABAergic pathway has been demonstrated in the turtle (Kenigfest et al, 2000(Kenigfest et al, , 2004. It arises in the nucleus lentiformis mesencephali and to a lesser extent in the nuclei griseus tectalis and pretectalis ventralis.…”

“…It arises in the nucleus lentiformis mesencephali and to a lesser extent in the nuclei griseus tectalis and pretectalis ventralis. In birds, the nuclei lentiformis mesencephali (pars magnocellularis and parvocellularis), griseus tectalis and principalis precommissuralis also project to the DLL (Gamlin and Cohen, 1988;Wild, 1989;Wylie et al, 1998); however, the GABAergic nature of this second pretectothalamic pathway, while highly probable (Kenigfest et al, 2000(Kenigfest et al, , 2004, has not been conclusively demonstrated by double labeling. The role played by the ascending GABAergic projection from the pretectal nuclei to the GLd/DLA is far from completely elucidated, although the involvement of the pretectum in visuomotor function and the integration of visual sensory and oculomotor function has been demonstrated in several studies (cf.…”

“…It is important to point out here that these different afferent supplies to the avian DLA, with the exception of the accessory optic system, have also been described in the GLd of reptiles (cf. Kenigfest et al, 1995Kenigfest et al, , 1998Kenigfest et al, , 2000Kenigfest et al, , 2004Kenigfest et al, , 2005Kenigfest et al, , 2006Belekhova et al, 2003) and mammals (cf. Niimi et al, 1970Niimi et al, , 1971Pasik et al, 1988Pasik et al, , 1990Raczkowski and Fitzpatrick, 1989;Papadopoulos et al, 1990;Harting et al, 1991a,b;Cucchiaro et al, 1991aCucchiaro et al, ,b, 1993Diamond et al, 1991;van der Want et al, 1992;Beaulieu and Cynader, 1992;Robson, 1993;Wilson, 1993;Feig and Harting, 1994;Montero, 1994;Vidnyanszky and Há mori, 1994;Feig et al, 1998;Wang et al, 2001Wang et al, , 2002Uhlrich et al, 2003).…”

“…Electron microscopic studies in reptiles (Kenigfest et al, 2004) and mammals (Partlow et al, 1977;Robson and Hall, 1977;Torrealba et al, 1981;Feig and Harting, 1994) have been undertaken to investigate the details of this projection, in particular the cytology of the terminals and their targets. In the turtle (Kenigfest et al, 2004) it has been shown that the tecto-geniculate terminals have the same cytological and immunological (GABA-immunonegativity and glutamate-immunopositivity) as corticogeniculate terminals, and have the same postsynaptic targets.…”

“…In the turtle (Kenigfest et al, 2004) it has been shown that the tecto-geniculate terminals have the same cytological and immunological (GABA-immunonegativity and glutamate-immunopositivity) as corticogeniculate terminals, and have the same postsynaptic targets. Corticogeniculate terminals having the same cytological and synaptological characteristics as the tecto-geniculate terminals of the turtle have been described in the squirrel (Robson and Hall, 1977), the galago (Feig and Harting, 1994), and the cat (Torrealba et al, 1981).…”