Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP

Abstract

The technique of intracellular recording and staining of the same neuron with horseradish peroxidase (HRP) was used to study the soma-dendritic and axonal morphology of nigrothalamic and nigrotectal cells in the rats. The nigrothalamic and nigrotectal cells were spread throughout the dorsoventral extent of the pars reticulata (SNR) and exhibited the same soma-dendritic and axonal features. Both populations consisted of medium-sized and large cells with extensive dendritic fields overlapping in all three directions. Their axons collateralized within the substantia nigra (SN) and in the mesencephalic tegmentum. The intrinsic collaterals were thin and branched partly within the dendritic field of a parent cell partly in remote regions of the SNR, and even in the pars compacta (SNC). The extrinsic branches involved thin arborizations in the rostroventral mesencephalic reticular substance and thicker descending and ascending collaterals. This material was supplemented by physiologically nonidentified HRP stained medium-sized and large neurons located in the SNR. The two kinds displayed the same extent and orientation of their dendrites but the branching patterns differed slightly. Proximal dendrites of all cells were coarse and smooth; thinner distal dendrites had varicosities and spinelike appendages. Some dendrites, specially those near the crus cerebri, terminated in dendritic thickets bearing many pleomorphic appendages. The orientation of dendritic fields varied with dorsoventral position of cells within the SNR. The most ventral region of the SNR contained neurons with dendrites oriented parallel to the crus cerebri and thus remained confined to the deepest stratum. The dendrites of cells in the central region of SNR were oriented mainly anteroposteriorly and ventrally, the ventral dendrites terminating in the ventralmost layer. Cells in the dorsolateral part of the SNR were characterized by the large dorsoventral extent of their dendrites which penetrated the entire thickness of SN. This variation in the arrangement of dendritic fields indicates that the SN is organized in three dorsoventral layers.

The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems

“…Sources of inputs to dopaminergic neurons that project to the matrix are still being examined, but so far have been thought to include the nucleus accumbens, ventral pallidum, lateral hypothalamus, lateral habenula, and amygdala (Nauta et al, 1978;Herkenham and Nauta, 1979;Christoph et al, 1986). These dopaminergic neurons may also receive an input from other parts ofthe subtantia nigra (Grofova et al, 1982). A number of studies suggest that nigrostriatal efferent activity may be regulated, in part, by GABAergic inputs from the pars reticulata (Dray et al, 1976;Grace and Bunney, 1979;Kamata et al, 1986).…”

“…The manner in which this organization is related to the pharmacological and physiological differences between subsets of dopaminergic neurons, which are thought to reflect differential affects of dopaminergic systems on movement and mood (Chiodo and Bunney, 1983;Creese, 1983;White and Wang, 1983), is discussed in the following paper (Gerfen et al, 1987), in which a biochemical marker is shown to dissociate the 2 dopaminergic systems. Grofova (1982) Neural interactions in the substantia nigra pars reticulata through axon collaterals of the projection neurons. Exp.…”

Synaptic organisation of the basal ganglia

“…Thus individual output neurons of the basal ganglia as well as neurons of the STN and dopaminergic neurons receive convergent input from pallidal afferents carrying motor\associative information and limbic information. Another way by which basal ganglia output neurons and STN neurons may integrate functionally diverse information from the pallidal complex is via their dendrites as they also receive pallidal inputs (Smith & Bolam, 1989 ;Bolam & Smith, 1992 ;Bevan et al 1996Bevan et al , 1997 and are often oriented to cross the functional boundaries defined by inputs from different functional divisions of the pallidal complex (Grofova et al 1982 ;Kita et al 1983 ;Nakanishi et al 1991 ;Bevan et al 1997). …”

The striatofugal fiber system in primates: A reevaluation of its organization based on single-axon tracing studies

“…Because striosomes are known to be innervated by cortical areas and subcortical structures related to the limbic system (7,12,46,47), SNr could play a role in the integration of limbic, cognitive, and sensorimotor information. Furthermore, because SNr neurons exhibit extensive local axon collateral networks innervating dopaminergic SNc neurons (44,(48)(49)(50), they could thus contribute to an indirect nigrostriatal loop circuit through which the striatum might up-regulate its level of dopaminergic transmission via a disinhibition of nigrostriatal neurons. This idea is supported by physiological studies showing a disinhibition of dopaminergic neurons after striatal stimulation or GABA agonist in SNr (51,52).…”