Elsevier

Neuroscience

Volume 24, Issue 2, February 1988, Pages 379-431
Neuroscience

Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography

https://doi.org/10.1016/0306-4522(88)90339-9Get rights and content

Abstract

The aim of the present study was to determine the organization of the afferents of the mediodorsal thalamic nucleus in relation to the reciprocal connections of this nucleus with different areas of the prefrontal cortex. For this purpose injections of horseradish peroxidase, or horseradish peroxidase conjugated to wheatgerm agglutinin were placed in different parts of the mediodorsal nucleus. These experiments revealed the organization of the reciprocal mediodorsal-prefrontal connections since wheatgerm agglutinin-horseradish peroxidase is transported effectively in anterograde and retrograde directions. Injections of wheatgerm agglutinin-horseradish peroxidase or fluorescent tracers were placed in different portions of the prefrontal cortex and the lectin Phaseolus vulgaris leucoagglutinin was injected in the mediodorsal nucleus in order to verify in more detail the point-to-point relationship in the mediodorsal-prefrontal connections. The organization of a number of the subcortical afferents to the mediodorsal nucleus was determined in detail using injections of Phaseolus vulgaris leucoagglutinin, wheatgerm agglutinin-horseradish peroxidase, or tritiated amino acids in areas identified as a source of mediodorsal afferents in the retrograde tracing experiments. These anterograde tracers were injected in different parts of the pallidal complex, the amygdala, the lateral hypothalamus, the lateral entorhinal cortex, the ventral mesencephalon, the superior colliculus and the dorsal tegmental region.

The results of the present experiments indicate that the mediodorsal nucleus, on the basis of its cyto-myelo- and chemoarchitecture as well as the organization of its reciprocal connections with the prefrontal cortex, can be subdivided into a medial, a central, a lateral and a paralamellar segment. Apart from this subdivision along a mediolateral axis, rostrocaudal and dorsoventral differences are also evident in the structural organization and connectivity of the mediodorsal nucleus.

A number of subcortical structures send fibres to all parts of the mediodorsal nucleus. The reticular thalamic nucleus projects to the mediodorsal nucleus in a topographical way such that its rostral part is connected with the rostral part of the nucleus, whereas more caudal and ventral areas in the reticular thalamic nucleus are connected with more caudal parts of the mediodorsal nucleus. Regions in the brainstem that project to all parts of the mediodorsal nucleus include the mesencephalic raphénuclei, the locus coeruleus, the rostral part of the central gray substance and the reticular formation. The median raphénucleus projects most heavily to lateral parts of the mediodorsal nucleus, whereas the dorsal raphénucleus is most strongly connected with its medial parts.

Besides these general inputs, the different mediodorsal nuclear segments receive a specific input and have different relations with particular areas of the prefrontal cortex. The rostral part of the medial segment of the nucleus is reciprocally connected mainly with the prelimbic and the ventral anterior cingulate areas, and to a lesser degree with the medial orbital and the ventral agranular insular areas. The posterior, ventral part of the medial segment of the mediodorsal nucleus has reciprocal fibre relations with the dorsal agranular insular area. The most medial part of the nucleus, immediately adjacent to the paraventricular nucleus, receives fibres from the infralimbic area, but appears not to reciprocate them. The medial segment receives input from a large number of structures in the realm of the limbic system, i.e. the amygdala, the lateral entorhinal cortex, the nucleus of the diagonal band of Broca, the lateral preoptic area, the supramammillary nuclei and from structures that are closely related to the basal ganglia system, i.e. the ventral pallidum, the ventral tegmental area and the pars reticulata of the substantia nigra. With an antibody against dopamine, it was determined that both the paraventricular nucleus and the adjacent parts of the mediodorsal nucleus contain a plexus of dopaminergic fibres. The most medial zone of the dorsal-medial thalamus, which includes the paraventricular nucleus, receives additional fibres from the nucleus accumbens, the bed nucleus of the stria terminalis, the dorsomedial hypothalamus, the subiculum, the parabrachial nuclei and the nucleus of the solitary tract.

The central segment of the mediodorsal nucleus differs from the medial segment in that it receives its most strong and specific input from olfactory related structures, such as the deep layers of the prepiriform cortex and the ventral pallidal cells in the olfactory tubercle. The central segment also receives afferents from the nucleus of the diagonal band of Broca, the lateral preoptic area and the lateral hypothalamus. This segment of the nucleus is reciprocally connected with the ventral agranular insular and the lateral orbital areas. The lateral segment of the mediodorsal nucleus receives a small number of fibres from the medial portion of the globus pallidus and the lateral hypothalamus, but its main inputs come from brainstem structures such as the substantia nigra, pars reticulata, the interpeduncular nucleus and the dorsolateral tegmental nucleus. This segment of the nucleus is reciprocally connected mainly with the dorsal anterior cingulate area. The paralamellar segment of the mediodorsal nucleus receives afferents from the deep layers of the superior colliculus, the pars reticulata of the substantia nigra and the dorsolateral tegmental nucleus. Additional inputs most probably come from pretectal nuclei, the region of the cuneiform nucleus and the contralateral fastigial nucleus of the cerebellum. This segment of the nucleus is reciprocally connected with the medial precentral area of the frontal cortex, an area that in the rat constitutes the frontal eye field. These results indicate that in the rat, via distinct segments of the mediodorsal thalamic nucleus, different parts of the prefrontal cortex can be influenced by a wide spectrum of structures that are mainly involved in the limbic circuitry, or are part of the limbic-afferented basal ganglia. An important observation is that the mediodorsal nucleus receives strong inputs from pallidal, nigral and tectal areas, which are the main waystations in the outflow of the basal ganglia. This may imply a role for the mediodorsal nucleus in the anticipatory and corollary mechanisms that have been alluded to the prefrontal cortex.

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