Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum

Abstract

The organization of the thalamic projections to the ventral striatum in the rat was studied by placing injections of the retrograde tracer cholera toxin subunit B in the ventral striatum and small deposits of the anterograde tracer Phaseolus vulgaris‐leucoagglutinin (PHA‐L) in individual midline and intralaminar thalamic nuclei. In order to provide a complete map of the midline and intralaminar thalamostriatal projections, PHA‐L injections were also made in those parts of the intralaminar nuclei that project to the dorsal striatum. The relationship of thalamic afferent fibres with the compartmental organization of the ventral striatum was assessed by combining PHA‐L tracing and enkephalin immunohistochemistry. The various midline and intralaminar thalamic nuclei project to longitudinally oriented striatal sectors. The paraventricular thalamic nucleus sends most of its fibres to medial parts of the nucleus accumbens and the olfactory tubercle, whereas smaller contingents of fibres terminate in the lateral part of the nucleus accumbens and the most ventral, medial, and caudal parts of the caudate‐putamen complex. The projections of the parataenial nucleus are directed towards central and ventral parts of the nucleus accumbens and intermediate mediolateral parts of the olfactory tubercle. The intermediodorsal nucleus projects to lateral parts of the nucleus accumbens and the olfactory tubercle and to ventral parts of the caudate‐putamen. The projection of the rhomboid nucleus is restricted to the rostrolateral extreme of the striatum. A diffuse projection to the ventral striatum arises from neurons ventral and caudal to the nucleus reuniens rather than from cells inside the nucleus. Fibres from the central medial nucleus terminate centrally and dorsolaterally in the rostral part of the nucleus accumbens and medially in the caudate‐putamen. Successively more lateral positions in the caudate‐putamen are occupied by fibres from the paracentral and central lateral nuclei, respectively. The lateral part of the parafascicular nucleus projects to the most lateral part of the caudate‐putamen, whereas projections from the medial part of this nucleus terminate in the medial part of the caudate‐putamen and in the dorsolateral part of the nucleus accumbens. Furthermore, a rostral to caudal gradient in a midline or intralaminar nucleus corresponds to a dorsal to ventral and rostral to caudal gradient in the striatum. In the ventral striatum, thalamic afferent fibres in the “shell” region of the nucleus accumbens avoid areas of high cell density and weak enkephalin immunoreactivity. In the “core” region of the nucleus accumbens and in the adjacent ventral part of the caudate‐putamen, thalamostriatal fibres generally avoid areas of strong enkephalin immunoreactivity, with the exception of fibres originating in the paraventricular and rhomboid nuclei which rather selectively concentrate inside these areas. The present findings demonstrate a precise topographical organization of the thalamostriatal projections originating in the midline and intralaminar nuclei of the rat. In combination with the available data on the afferents of these nuclei, the observations are in support of the presence of several, functionally different sectors within the striatu m. Furthermore, the relationship of the thalamostriatal projections with the neurochemical compartmentation of the ventral striatum, identified by enkephalin immunohistochemistry, provides a connectional basis for these compartments.