Topographical organization of efferent projections from the cat substantia nigra pars reticulata

Abstract

The topographical organization of the efferent projections from the cat substantia nigra (SN) to the thalamus and the superior colliculus was examined using the anterograde transport of horseradish peroxidase—wheat germ agglutinin (HRP-WGA) and of labelled proteins. HRP-WGA or a mixture of [ 14C]amino acids was injected into various areas of the SN and the transported material visualized on coronal brain sections by histochemistry or autoradiography, respectively. The retrograde transport of [ 14C]γ-aminobutyric acid ([ 14C]GABA) injected into thalamic nuclei was used also to determine the identity of the nigrothalamic projections. Identical results were found using either the anterograde transport of HRP-WGA or of labelled proteins. In the thalamus, dense nigral projections were observed in the nucleus ventralis medialis (VM) and in the rostromedioventral part of the nucleus ventralis lateralis (VL) whilst more limited projections were seen in the nuclei centralis lateralis (CL) and paracentralis (PC) as well as in the paralamellar zone of the nucleus medialis dorsalis (MD-Il). In addition, a patchy distribution of HRP-WGA or of radioactivity was found in the intermediate layer of the superior colliculus. More precisely, labelling of the VM was dense following injection of [ 14C]amino acids into the intermediate part of the SN pars reticulata (SNR) regardless of the depth of the injection site, whilst the intralaminar nuclei were labelled preferentially following injections made into the dorsal part of the intermediate SNR. Nigral projections to the intermediate layer of the superior colliculus were visualized over the whole mediocaudal and laterorostral extent when [ 14C]amino acids were injected into the rostral part of the SNR. Labelling of the superior colliculus was also seen following injection of [ 14C]amino acids into the intermediate part of the SNR but, in this case, ventral injections led to a more intense labelling than dorsal ones. Both the SNR and the SN pars compacta (SNC) were labelled when [ 14C]GABA was injected into the VM nucleus of the thalamus, confirming that the nigro VM projection is GABAergic and showing that recurrent collaterals of these GABAergic cells innervating the SNC also contained the transported radioactive material. In this condition ([ 14C]GABA injection into the VM), the thalamic reticularis nucleus also exhibited a dense labelling. On the other hand, no labelling was observed in the SN (either SNR or SNC) when [ 14C]GABA was injected into the CL or the MD-Il, suggesting that the nigral projections to these thalamic nuclei are non-GABAergic. However, [ 14C]GABA injection into the CL did label the thalamic reticularis nucleus and the superior colliculus, suggesting that these structures send GABAergic projections to the CL.