Immunocytochemical localization of glutamic acid decarboxylase in normal and deafferented superior colliculus: evidence for reorganization of gamma-aminobutyric acid synapses

Abstract

There is circumstantial evidence that GABAergic synaptic terminals in the superior colliculus might become reorganized in response to a loss of the retinal innervation of this brain region. The present investigation tests this possibility by identifying y-aminobutyric acid (GABA) neurons and their synaptic relationships with an immunocytochemical localization of the GABA-synthesizing enzyme, glutamic acid decarboxylase (GAD), and by comparing these synaptic relationships in normal superior colliculus with those present 6 and 16 weeks after unilateral eye removal. In normal superior colliculus, light microscopy revealed a much denser concentration of GAD-positive reaction product in the superficial layers than in the intermediate and deep collicular layers. Most of this reaction product was contained within small, punctate structures, but GAD-positive somata and proximal dendrites also were observed. Electron microscopy showed that GAD was localized in numerous synaptic terminals, including those that were the presynaptic elements of dendrodendritic synapses. The vast majority of GAD-positive presynaptic elements formed symmetric synaptic junctions. In addition, GAD-positive profiles frequently were postsynaptic to unstained retinal terminals as well as presynaptic to unstained dendritic profiles and thus participated in serial synaptic relationships. Furthermore, both retinal and GAD-positive elements commonly were presynaptic to the same postsynaptic dendrite, and often these synaptic contacts were adjacent to each other. In deafferented specimens, profiles with the characteristics of retinal axon terminals were not observed, whereas there appeared to be no reduction of GAD-positive synaptic profiles. However, there was a marked and statistically significant increase in the proportion of GADpositive presynaptic terminals that formed asymmetric synaptic contacts in superior colliculus deprived of retinal input. This change indicates that partial deafferentation induces a reorganization of GAD-positive synapses. The long-term presence of the GABA-synthesizing enzyme within reorganized synaptic terminals also suggests that such presynaptic elements could produce and, presumably, release neurotransmitter.Previous investigations have sought evidence in a number of different brain regions for lesion-induced synaptic reorganization of neurons that use y-aminobutyric acid (GABA) as a neurotransmitter, but such alterations still remain to be demonstrated unequivocally.

GABAergic innervation of rat abducens motoneurons retrogradely labelled with HRP: quantitative ultrastructural analysis of cell bodies and proximal dendrites

“…In the literature, GABA axon terminals have been described by some authors as establishing exclusively symmetrical synaptic junctions (Somogyi et al, 1985;Somogyi & Solt6sz, 1986;Van der Want & Nunes Cardozo, 1988;Maxwell et al, 1989;Beaulieu & Somogyi, 1990). The GABA axon terminals we observed established mostly symmetrical junctions but also some asymmetrical synaptic junctions as has been previously described in various parts of the CNS (Ribak et al, 1979;Houser et al, 1983;Sotelo et al , 1986;Decavel & Van den Pol, 1990). Our quantitative estimation of the percentage of symmetrical junctions versus asymmetrical was slightly lower (85%) than the estimation given for the GABA axon terminals contacting the perikarya in the inferior olive (92-97%;De Zeeuw et al, 1989), or the trigeminal motor nucleus (93%; Saha et al, 1991).…”

Synaptic circuitry in the retinorecipient layers of the optic tectum of the lamprey (Lampetra fluviatilis). A combined hodological, GABA and glutamate immunocytochemical study

“…In mammals, the majority of the GABAergic terminals of the retinorecipient layers of the superior colliculus contain pleiomorphic vesicles and make symmetrical synaptic contact (cf. Lund 1969Lund , 1972Tigges et al 1973;Valverde 1973;Houser et al 1983;Mize 1992). However, Houser et al (1983) consider that in the retinorecipient layers of the rat superior colliculus 4% of the GABAergic terminals make assymmetrical synaptic contacts.…”

“…Lund 1969Lund , 1972Tigges et al 1973;Valverde 1973;Houser et al 1983;Mize 1992). However, Houser et al (1983) consider that in the retinorecipient layers of the rat superior colliculus 4% of the GABAergic terminals make assymmetrical synaptic contacts. In the lamprey, as in Gnathostomes, the GABAergic terminals make synaptic contacts with the dendrites of efferent neurons, and also with the GABAergic DCSV of interneurons which may in turn be presynaptic to the dendrites of efferent neurons.…”

“…In many Gnathostomes, the DCSV of the superficial tectal or collicular layers are also postsynaptic in most cases to retinal terminals, but also to terminals with pleiomorphic synaptic vesicles (fish, Peyrichoux et al 1986;amphibians, Székely et al 1973;Ingham and Güldner 1981;Antal 1991;reptiles, Repérant et al 1981;Rio et al 1995;birds, Angaut and Repérant 1976;mammals, Lund 1969mammals, Lund , 1972Tigges et al 1973;Valverde 1973;Tigges and Tigges 1975;Graham and Casagrande 1980;Vrensen and de Groot 1977;Houser et al 1983;Mize et al 1991;Pinard et al 1991).…”

“…In mammals the DCSV have been described in a variety of terms; balloonlike dilatations (Sterling 1971), vesicle-filled spines (Lund 1969), spine-like appendages or spine-bearing dendrites (Mize 1988(Mize , 1992, gemmule-like dendritic excrescences (Houser et al 1983), or as varicose dendritic enlargements (Mize et al 1991). It follows from this that the profiles are interpreted as arising from dendritic spines, dendritic varicosities, or both of these.…”