Nigrothalamic projections and nigrothalamocortical pathway to the medial agranular cortex in the rat: Single- and double-labeling light and electron microscopic studies

Abstract

Although the rat medial agranular cortex (AGm) has been implicated in a variety of motor functions, the source of the afferents impinging upon thalamic neurons projecting to the AGm is not directly known. The main purpose of this study was to determine whether the AGm is a major recipient of the nigrothalamocortical pathway. This issue was addressed by two sets of experiments. First, the organization of the nigrothalamic projections was studied by light and electron microscopy following injections of the anterograde tracer Phaseolus vulgaris-leucoagglutinin (PHA-L) into the pars reticulata of the substantia nigra (SNR). The major finding of this study was the disclosure of a heretofore unknown projection to the rostromedial part of the ventral anterior-ventral lateral complex (VAL). This projection originates exclusively from the ventral portion of the SNR and is comparable in strength to the well-known nigrothalamic projection to the ventromedial nucleus (VM). Electron microscopic examination revealed differences in the synaptic organization of nigral terminals in the VAL and the VM. A large proportion of the labeled terminals in the VAL was involved in axosomatic synapses, whereas, in the VM, the axosomatic synapses were rare, and 67% of nigral terminals were found in contact with thin dendrites. To assess a possible disynaptic nigrothalamocortical pathway to the AGm, a double-labeling strategy combining PHA-L injections in the SNR and pressure injections of the retrograde tracer, cholera toxin subunit B (CTB) in the AGm was employed. The greatest density of CTB-labeled neurons was found in the rostral and central portion of the VAL, coincident with the nigrothalamic labeling originating from the ventral SNR. Electron microscopic analysis confirmed that some of the PHA-L-labeled terminals established synaptic contacts with the CTB-labeled cell bodies and large dendrites. In conclusion, our findings indicate that there exist two different nigrothalamocortical pathways through the motor thalamus in the rat. The SNR-VAL-AGm cortical projection may play a role in oculomotor functions, whereas the SNR-VM-cortical pathway has been implicated in arousal mechanisms.

Thalamic interaction between the input and the output systems of the basal ganglia

“…No significant differences were found between the ultrastructural characteristics of nigral and pallidal axon terminals, and both displayed a common pattern of synaptic innervation of their targets (Grofová and Rinvik, 1974;Kultas-Ilinsky et al, 1983;Kultas-Ilinsky and Ilinsky, 1990;Sidibé et al, 1997). These studies have shown that the main postsynaptic target of the afferent fibers are the postsynaptic dendrites of relay cells (Grofová and Rinvik, 1974;Kultas-Ilinsky et al, 1983;Kultas-Ilinsky and Ilinsky, 1990;Sidibé et al, 1997) or identified thalamocortical neurons (Kayahara and Nakano, 1996;Sakai et al, 1998).…”

“…3A with Fig. 3 from Sakai et al, 1998), and also in the rostral intralaminar and mediodorsal nuclei, where even a complementary pattern is hinted (see Fig. 3A-A%, B-B%; for methodological considerations see Lanciego et al, 1998).…”

“…The terminal fields of both pallidal and nigral afferents to the thalamus have been extensively studied in several species (see references in Sidibé et al, 1997;Sakai et al, 1998). In the primate thalamus, both the motor thalamus and the caudal intralaminar nuclei are well-developed, with architectonically distinct nuclei and subnuclei (Asanuma et al, 1983;Ilinsky and Kultas-Ilinsky, 1987;Stepniewska et al, 1994).…”

“…Abundant studies have dealt with the relationships between the output of the basal ganglia and the thalamocortical projection at different levels, and some of the more recent ones have compared the pallidal/nigral terminal fields vs. thalamocortical neurons, by means of either single or double-labeling techniques at the light and/or electron microscopic levels, or using transneuronal techniques (Schell and Strick, 1984;Ilinsky et al, 1985;Alexander et al, 1986;Groenewegen, 1988;Hoover and Strick, 1993;Kayahara and Nakano, 1996;Sakai et al, 1998). In contrast, little has been reported regarding the relationships between the output of the basal ganglia and the thalamic input to the striatum (de las Heras et al, 1997Heras et al, , 1998a.…”

Metabolic Mapping of the Effects of Win 55212–2 Intravenous Administration in the Rat

“…In this respect, there is evidence for the inhibition of hippocampal acethylcholine release by cannabinoids . Moreover, metabolic depression was measured in the ventromedial thalamic nucleus that has been implicated in arousal mechanisms (Sakai et al 1998).…”