Retinal and cortical afferents to the dorsal lateral geniculate nucleus of the turtle,Emys orbicularis: A combined axonal tracing, glutamate, and GABA immunocytochemical electron microscopic study

Abstract

The dorsal lateral geniculate nucleus (GLd) of the turtle Emys orbicularis has been analyzed with axonal tracing methods and immunocytochemical techniques for glutamate (GLU) and gamma-aminobutyric acid (GABA), in combination with a quantitative study of the morphologic characteristics, distribution, and synaptology of the retinofugal and corticofugal terminals. Ultrastructural observations show that the vast majority of retinal terminals (Rtr) have clear, rounded synaptic vesicles and account for 16% of all profiles containing synaptic vesicles (PCSV). Their synaptic index (0.5) is low, and they make three times more contacts with the dendrites of projection cells than with those of interneurons. A low proportion of retinal terminals of a second category contain pleomorphic synaptic vesicles and are highly GABA immunoreactive. Axon terminals, unlabeled after intraocular injection of the tracer (SR), smaller in size and with more rounded clear synaptic vesicles, longer synaptic differentiations, and higher synaptic index than Rtr terminals, account for 19.7% of all PCSV and make asymmetric synaptic contacts with large dendrites of projection cells and less with the dendrites of interneurons. Some SR have been unambiguously identified as corticofugal terminals (Cg), either after cortical injection of the tracer (16%) or cortical lesion (37%). Retinal and Cg/SR terminals are spatially segregated within the GLd. Both are highly GLU immunoreactive, with the highest density of labeling over synaptic vesicles, suggesting that these terminals may use GLU as neurotransmitter. The level of GLU immunoreactivity of GABA-positive profiles is half that of Rtr and Cg/SR terminals and is greatest over mitochondria, possibly reflecting the 'metabolic' pool of GLU that serves as a precursor in the formation of GABA.

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

“…Tracing studies have shown that a proportion (about 37%) of the SR terminals represents the corticogeniculate projection, and immunocytochemical studies have shown that all the Rtr and a large proportion of SR, including cortical terminals, are highly glutamate‐ir. Comparing our findings with those obtained by others (see references in Kenigfest et al, 1995, 1998) in birds and mammals reveals many important similarities in the fine structure of the GLd, particularly with respect to the cytological properties of retinal and cortical terminals, their targets, and their immunochemical properties.…”

“…Large arrows indicate thick and thin smooth fibers, small arrows indicate thin varicose fibers labeled in the cell plate (GLdc), in the inner (GLdin) and outer (GLdon) neuropil of the nucleus, and in the optic tract (TrO) either after pretectal (Kenigfest et al, 2000) or tectal (Belekhova et al, 2003) tracer injection. Gray areas represent unlabeled cell bodies of glutamatergic projection neurons in the cell plate, and open areas represent unlabeled cell bodies of GABAergic local neurons in the inner and outer neuropil and optic tract (Kenigfest et al, 1995, 1998). D and L, respectively, represent the dorsal and lateral axes of the brain.…”

“…Numerous light microscopic axonal tracing studies and electrophysiological experiments have shown that the dorsal lateral geniculate nucleus (GLd) of turtles receives an important, primarily contralateral, afferent supply from the retina and projects to the dorsal cortex of the telencephalon, which in turn projects back to the GLd (for review see Kenigfest et al, 1995, 1998). A sparse projection of the optic tectum to the GLd has also been demonstrated by several investigators (for review see Ulinski et al, 1992; Reiner, 1994; Belekhova et al, 2003).…”

“…We undertook (Kenigfest et al, 1995, 1998) a series of electron microscopic studies of the GLd of the turtle, with a view to describing its ultrastructure, in particular after labeling some of these afferent supplies with tracer and also after having carried out immunocytochemical studies in order to specify some properties of the components of this nucleus. We were also able to analyze the spatial relationships of these terminals, and to describe their postsynaptic targets, in the three principal subdivisions of the GLd (Ulinski, 1986), the medial cell plate and the lateral neuropil, the latter being divided into inner and outer regions.…”

Dual midbrain and forebrain origins of thalamic inhibitory interneurons

“…For example, in the reptilian thalamus, which is mostly devoid of descending projections from the cortex, interneurons have only been identified in the retinorecipient regions (Rio et al, 1992; Pritz and Stritzel, 1994; Kenigfest et al, 1995, 1998; Butler, 2008). In birds however, where reciprocal connections between the thalamus and the cortex are more abundant, thalamic interneurons are distributed more widely (Granda and Crossland, 1989; Veenman and Reiner, 1994; Butler, 2008).…”