An ultrastructural double‐label immunohistochemical study of the enkephalinergic input to dopaminergic neurons of the substantia nigra in pigeons

Abstract

Electron microscopic immunohistochemical double-label studies were carried out in pigeons to characterize the ultrastructural organization and postsynaptic targets of enkephalinergic (ENK+) striatonigral projection. ENK+ terminals in the substantia nigra were labeled with antileucine-enkephalin antiserum by using peroxidase-antiperoxidase methods, and dopaminergic neurons were labeled with anti-tyrosine hydroxylase antiserum by using silver-intensified immunogold methods. ENK+ terminals on dopaminergic neurons were equal in abundance to ENK+ terminals on nondopaminergic neurons, although the former were typically somewhat smaller than the latter (mean size: 0.50 vs. 0.75 micron, respectively). ENK+ terminals were evenly distributed on the cell bodies and dendrites of dopaminergic neurons, and they were evenly distributed on dendrites but rare on perikarya of nondopaminergic neurons. Transection of the basal telencephalic output revealed that 75% of the nigral ENK+ terminals were of basal telencephalic origin. These telencephalic ENK+ terminals included over 80% of those smaller than 0.80 micron on dopaminergic neurons and smaller than 1.0 micron on nondopaminergic neurons, and none greater than this in size. Both telencephalic and the nontelencephalic ENK+ nigral terminals made predominantly symmetric synapses on nigral neurons. Although the basal telencephalic ENK+ terminals uniformly targeted dendrites and perikarya, nontelencephalic ENK+ terminals seemed to avoid perikarya. The results indicate that ENK+ striatonigral neurons in birds may directly influence both dopaminergic and nondopaminergic neurons of the substantia nigra. Based on similar data for substance P-containing striatonigral terminals, the roles of enkephalin and substance P in influencing nigral dopaminergic neurons may differ slightly, as they appear to target preferentially different portions of dopaminergic neurons. The overall results in pigeons are similar to those for ENK+ terminals in the ventral tegmental area in rats, suggesting that the synaptic organization of the ENK+ input to the tegmental dopaminergic cell fields is similar in mammals and birds.

Abundance and location of DARPP-32 in striato-tegmental circuits of domestic chicks

“…The claim that the juxtapositions observed in the present study represent genuine synapses can be substantiated by previous electron microscopic studies (Karle et al, 1992 demonstrating that TH+ terminals make synaptic contact with the same type of striatal neurons as those containing DARPP-32. Similarly, the juxtapositions observed by us in the tegmental dopaminergic nuclei likely correspond to those substance P or enkephalin-containing terminals, which have been shown to form synaptic junctions with dopaminergic neurons of the nigra Medina et al, 1995).…”

“…Synaptic contacts between dopaminergic nigral and AVT neurons and striatal fibres have been verified in mammals (Smith and Bolam, 1990) and also in birds , Medina et al, 1995. The dopamine containing projection arising from the brainstem profusely innervates the basal ganglia including the MSt (part of which is likely to represent also the avian nucleus accumbens, see Mezey and Csillag, 2002) and the LSt.…”

The avian subpallium: New insights into structural and functional subdivisions occupying the lateral subpallial wall and their embryological origins

“…These projection neurons possess spiny dendrites, and about half also contain enkephalin while the other half show colocalization of substance P (SP) and dynorphin (Brauth et al, 1983; Reiner et al, 1983, 1984; Reiner and Anderson, 1990; Anderson and Reiner, 1990a; Anderson and Reiner, 1991; Veenman and Reiner, 1994; Sun et al, 2005). These neurons account for the SP+ and enkephalinergic projections of MSt to the dopaminergic neurons of the substantia nigra pars compacta and the GABAergic neurons of the substantia nigra pars reticulata (Anderson et al, 1991; Medina et al, 1995; Veenman and Reiner, 1994), of which the SP+ projection is more prominent. The MSt neurons projecting to the substantia nigra and the ventral tegmental area send their axons through the ventral pallidum, and some have terminations there (Kitt and Brauth, 1981; Medina and Reiner, 1997; Person et al, 2008).…”

“…Corticopetal cholinergic neurons play an important role in modulation of cortical activity, and in attentional and arousal processes (Záborszky et al, 1999) that affect learning and memory (Metherate et al, 1988, 1992; Cape and Jones, 2000; Cape et al, 2000). Similarly, the avian corticopetal system consists of scattered large cholinergic neurons that are dispersed over the pallidum-substantia innominata, and septal-diagonal band regions (Medina and Reiner, 1994; Medina et al, 1995). In birds, telencephalic structures containing cholinergic neurons (Reiner et al, 2004a) include the basal magnocellular nucleus (NBM, Fig.…”

Organization of the dopaminergic innervation of forebrain areas relevant to learning: A combined immunohistochemical/retrograde tracing study in the domestic chick

“…The demonstration of retrogradely labeled DA-ir neurons in the mesencephalic nuclei AVT and SN after tracer injections into the MNH, Ndc, and LPO provides the first direct evidence that the dopaminergic innervation of the avian forebrain arises from these nuclei. The presence of retrogradely labeled neurons in AVT and SN that display no immunoreactivity for DA indicates that there are neuronal populations within these nuclei that do not use DA as transmitter (see also Medina et al, 1995).…”