The postsynaptic targets of substance P-immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons

Abstract

Substance P-immunoreactive boutons were examined in the electron microscope in sections of the rat neostriatum that contained retrogradely labelled striatonigral neurons and/or Golgi-impregnated medium-size densely spiny neurons. The post-synaptic targets of the immunoreactive boutons were characterized on the basis of ultrastructural features, their projection to the substantia nigra and/or their somato-dendritic morphology. Substance P-immunoreactive axonal boutons formed symmetrical synaptic specializations. Of a total of 233 randomly identified synaptic boutons 72.5% made contact with dendritic shafts, 15% with dendritic spines and 10.7% with perikarya. The ultrastructural characteristics of some of the postsynaptic neuronal perikarya were consistent with their identification as striatal interneurons. Similarly, the observation of some of the substance P-containing terminals in contact with spines, spine-bearing dendritic shafts and perikarya with the ultrastructural characteristics of medium-size densely spiny neurons suggested that one of the targets of substance P-positive terminals are striatal projection neurons. Direct evidence for this was obtained in sections from rats that had received injections of horseradish peroxidase conjugated with wheatgerm agglutinin in the substantia nigra. The perikarya of retrogradely labeled striatonigral neurons were found to receive symmetrical synaptic input from substance P-positive boutons. Ultrastructural analysis of Golgi-impregnated medium-size densely spiny neurons, some of which were also retrogradely labeled from the substantia nigra, demonstrated directly that this class of neuron was postsynaptic to the substance P-immunoreactive boutons. The combination of Golgi-impregnation with substance P-immunocytochemistry made it possible to study the pattern or topography of the substance P-positive input to medium size densely spiny neurons. The substance P-containing boutons made contact predominantly with perikarya and dendritic shafts. This pattern of input is markedly different from that of other identified inputs to medium-size densely spiny neurons.

Dopaminergic Modulation of Axon Collaterals Interconnecting Spiny Neurons of the Rat Striatum

“…This is supported by a recent preliminary report using pair recordings with high intracellular chloride to enhance unitary IPSCs (Koos et al, 2002), as well as by other indirect studies (Rebec and Curtis, 1988). It was shown that neurons immunoreactive for SP and ENK received GABAergic synapses modulated by either D 1 or D 2 receptor agonists, suggesting that pathways containing one or both receptor types (Gerfen et al, 1990;Gerfen, 2000) communicate with one another (Aronin et al, 1986;Bolam and Izzo, 1988;Gerfen and Young, 1988;Yung et al, 1996).…”

“…Inhibition comes from two main sources: interneurons (Kita, 1993;Bennett and Bolam, 1994;Jaeger et al, 1994;Kawaguchi et al, 1995;Koos and Tepper, 1999) and recurrent axon collaterals interconnecting projection neurons (Park et al, 1980;Wilson and Groves, 1980;Somogyi et al, 1981;Bishop et al, 1982;Groves, 1983;Aronin et al, 1986;Bolam and Izzo, 1988;Czubayko and Plenz, 2002;Koos et al, 2002;Tunstall et al, 2002). We asked whether dopamine regulates the strength of synapses between projection neurons.…”

“…The globus pallidus (GP) was first lesioned with ibotenic acid to destroy intrinsic pallidal cells. Related questions were whether modulation produced by D 1 receptor agonists is different from, or even opposed to, that produced by D 2 receptor agonists (Floran et al, 1990(Floran et al, , 1997Radnikow and Misgeld, 1998;Cooper and Stanford, 2001) and whether spiny neurons from the direct and the indirect pathways (Gerfen and Young, 1988;Albin et al, 1989) are synaptically interconnected (Aronin et al, 1986;Bolam and Izzo, 1988;Yung et al, 1996).…”

Local circuit neurons in the striatum regulate neural and behavioral responses to dopaminergic stimulation

“…NK-1 receptors in the striatum are expressed principally by the cholinergic and NOS interneurons, but low levels of NK-1 receptor expression (22) and some direct NK-1 receptormediated effects (23) have been reported for SP-immunoreactive projection neurons themselves, suggesting the presence of NK-1 autoreceptors. We therefore tested for changes in the numbers of striatal projection neurons within the SP-PE35 injection sites.…”

D1 and D2 dopamine receptor function in the striatum: coactivation of D1- and D2-dopamine receptors on separate populations of neurons results in potentiated immediate early gene response in D1-containing neurons

“…Immunohistochemical data suggest that Dland D2-containing neurons are in fact interconnected (Hersch et al, 1995). Electron microscopic ultrastructural localization of peptides such as substance P and enkephalin, which are markers of Dl and D2 neurons, respectively, have demonstrated contacts between these different neuron types (Bolam and Izzo, 1988). Thus, there appear to exist synaptic contacts between D2-and Dl -containing neurons.…”