Anthony H. M. Lohman

Chapter 5 The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization

Recent findings in primates indicate that the connections of the frontal lobe, the basal ganglia, and the thalamus are organized in a number of parallel, functionally segregated circuits. In the present account, we have focused on the organization of the connections between the prefrontal cortex, the basal ganglia and the mediodorsal thalamic nucleus in the rat. It is concluded that in this species, in analogy with the situation in primates, a number of parallel basal ganglia-thalamocortical circuits exist. Furthermore, data are presented indicating that the projections from particular parts of the amygdala and from individual nuclei of the midline and intralaminar thalamic complex to the prefrontal cortex and the striatum are in register with the arrangements in the parallel circuits. These findings emphasize that the functions of the different subregions of the prefrontal cortex cannot be considered separately but must be viewed as components of the integrative functions of the circuits in which they are involved.

Cortical afferents of the nucleus accumbens in the cat, studied with anterograde and retrograde transport techniques.

The cortical afferentation of the nucleus accumbens in the cat was studied with the aid of retrograde tracing techniques. Retrograde experiments were carried out with horseradish peroxidase or one of the fluorescent tracers Bisbenzimid, Nuclear Yellow and Fast Blue. In the anterograde experiments [3H]leucine and [35S]methionine were used as tracers. Following injections in the nucleus accumbens, retrogradely-labelled cells were found in the medial frontal cortex, the anterior olfactory nucleus, the posterior part of the insular cortex, the endopiriform nucleus, the amygdalo-hippocampal area, the entorhinal and perirhinal cortices and the subiculum of the hippocampal formation. In the medial frontal cortex most of the labelled cells were found in layers III and V of the prelimbic area (area 32 of Brodmann), but retrogradely-filled neurons were also present in the infralimbic area and in the caudoventral part of the lateral bank of the proreal gyrus. Retrogradely-labelled cells in the entorhinal and perirhinal cortices were located in the deep cellular layers. Following large injections in the nucleus accumbens, retrograde labelling in the subiculum extended from the most dorsal, septal pole to the most ventral, temporal pole. Injections of anterograde tracers were placed in the frontal cortex, the entorhinal and perirhinal cortices and the hippocampal formation. The prelimbic area was found to project via the internal capsule to mainly the rostral half of the nucleus accumbens, whereas in the caudal half of the nucleus only a lateral region receives frontal cortical fibres. Following injections in the infralimbic area only fibres passing through the nucleus accumbens were labelled. Afferents from the entorhinal and perirhinal cortices reach the nucleus accumbens by way of the external capsule and terminate mainly in a ventral zone of the nucleus accumbens. Afferents from the entorhinal area are distributed to the entire accumbens, whereas the termination field of the perirhinal afferents is largely restricted to the lateral part of the nucleus accumbens. Both the frontal cortex and the entorhinal and perirhinal cortices appear to project also to the nucleus caudatus and the tuberculum olfactorium. These cortical areas also project to the contralateral striatum. Both anterograde and retrograde tracing experiments demonstrated a topographical relationship between the subiculum and the nucleus accumbens. The ventral pole of the subiculum projects via the fornix to the medial part of the caudal half of the nucleus accumbens and to a small dorsomedial area in its rostral half. Successively more dorsal portions in the subiculum project to successively more ventrolateral parts in the rostral nucleus accumbens. The projection from the hippocampus was found to extend also to the tuberculum olfactorium. The results of the present study do not provide unambiguous criteria for the delimitation of the nucleus accumbens in the cat.

Reciprocal connections of the insular and piriform claustrum with limbic cortex: An anatomical study in the cat

The connections of the claustrum with non-isocortical limbic and paralimbic cortex in the cat are described, using the anterograde transport of tritiated amino acids and the retrograde transport of various fluorescent tracers and of horseradish peroxidase conjugated to the lectin wheatgerm agglutinin. It could be demonstrated that the claustrum, in addition to its connections with sensory-related areas, is reciprocally and bilaterally connected with widespread limbic and paralimbic cortical regions. These connections are organized such that the area of origin of claustral efferents to a certain cortical region coincides with the area of termination in the claustrum of afferents from that same cortical region. A rostrocaudal topographical organization of the limbic-related connections of the claustrum is not very apparent. However, the results clearly demonstrate a dorsoventral topographical organization in the connections between the claustrum and the cortex. The ventral part of the claustrum has reciprocal connections predominantly with the entorhinal cortex, and possibly with the anterior olfactory nucleus and the prepiriform cortex. A more dorsally located part of the claustrum is preferentially connected with the orbitofrontal, the insular, the perirhinal, the anterior limbic, and the cingular cortices, and with parts of the subicular complex. The most dorsal portion of the claustrum is more heavily connected with parasensory and sensory cortices. It is concluded that the traditional subdivision of the claustrum into two discrete nuclei, i.e. the insular claustrum connected with the isocortex, and the piriform claustrum or endopiriform nucleus connected with the allocortex, does not reflect the actual organization of the cortical connections of the claustrum. The present data provide a more differentiated view, such that the ventral portion of the claustrum is reciprocally connected mainly with the olfactory-related cortices and the entorhinal cortex, whereas the cortical connections of progressively more dorsal parts of the claustrum gradually shift from limbic and paralimbic towards parasensory and sensory cortical connections. The significance of these findings is discussed in the light of a possible function of the claustrum in relation to corticocortical integration and memory processing.

Afferent connections of the striatum and the nucleus accumbens in the lizard Gekko Gecko

The efferent connections of the striatum and the nucleus accumbens of the lizard Gekko gecko were studied with the anterograde tracer Phaseolus vulgaris-leucoagglutinin (PHA-L). These structures were found to have segregated output systems. The striatum shows a major projection to the globus pallidus. Striatal fibers which are more caudally directed run through the lateral forebrain bundle and can be traced as far caudally as the pars reticularis of the substantia nigra where they exhibit many varicosities. Along its course, the lateral forebrain bundle issues fibers with varicosities to the anterior and posterior entopeduncular nuclei. The major recipient structure of the nucleus accumbens is the ventral pallidum. The nucleus accumbens, in addition, projects to the portion of the lateral hypothalamus in the path of the medial forebrain bundle and to the ventral tegmental area, which is its most caudal target. Subsequently, the same technique was used in an attempt to study the efferents of the globus pallidus and the ventral pallidum, the major recipient structures of the striatum and the nucleus accumbens. The globus pallidus was found to project to the rostral part of the suprapeduncular nucleus in the ventral thalamus and, in addition, may distribute fibers to the same structures as does the striatum. The ventral pallidum distributes fibers to the ventromedial thalamic nucleus. It probably also projects diffusely to the hypothalamus, the habenula, and the mesencephalic tegmentum.

Overview of the Main and Accessory Olfactory Bulb Projections in Reptiles

The present account is a review of the main and accessory olfactory bulb projections in reptiles. From previous studies by means of the classical degeneration techniques and recent studies using the autoradiographic method or the Phaseolus vulgarus-leucoagglutinin (PHA-L) tracing technique, it has become evident that, in the brain of reptiles, the vomeronasal and main olfactory systems are segregated. Moreover, the PHA-L studies have demonstrated that the main olfactory bulbs project not only to the anterior olfactory nucleus, the olfactory tubercle, and the lateral cortex, but also to the rostral portions of the external and central amygdaloid nuclei. The latter studies also provided evidence that, apart from a massive projection to the nucleus sphericus, at least in some reptilian species, the accessory olfactory bulbs project to the caudal portion of the central amygdaloid nucleus and the bed nucleus of the stria terminalis. A comparison of the olfactory projections between the various reptilian species studied revealed a considerable variation in the course of the main olfactory bulb efferents that reach the contralateral hemisphere.

The Dorsal Ventricular Ridge and Cortex of Reptiles in Historical and Phylogenetic Perspective

From a comparative point of view, reptiles are of particular interest, since they are believed to be ancestral to both birds and mammals. It is, therefore, not surprising that in many laboratories species of the reptilian class have been and are still being used in search for basic features of the central nervous system of amniotes, i.e. reptiles, birds, and mammals. One of the most intriguing questions is whether a structure homologous to the mammalian neocortex is already present in the forebrain of reptiles. Before dealing with this question, some introductory comments will be made on the classification of the reptilian species mentioned in this chapter and on the anatomy of the reptilian forebrain.

On the Basal Ganglia of a Reptile: The Lizard Gekko Gecko

Since reptiles possess markedly developed basal ganglia, quite some attention has been paid to the comparison of the organization of these structures with that in mammals. The presumed homologue of the mammalian nucleus accumbens and corpus striatum (caudate nucleus, putamen, and globus pallidus) is in reptiles generally referred to as the paleostriatum (Ariens Kappers et al., 1936). Within the paleostriatum most investigators recognize a laterally located striatum and a medially located nucleus accumbens (e.g. Northcutt, 1981). The so defined striatum can be subdivided into a rostral parvocellular part and a caudal magnocellular part. Further, ventrolaterally located large cells of the caudal part have been compared to the large cells of the mammalian globus pallidus (Holmgren, 1922), and Kallen (1951, 1962), on the basis of embryological arguments, in fact homologized this ventrolateral area of the reptilian striatum with the globus pallidus of mammals. The existence of a distinct structure in the striatum was confirmed by histochemical techniques (e.g. succinate dehydrogenase, Baker-Cohen, 1968; acetylcholinesterase and catecholamines, Parent and Olivier, 1970). At that time little was known about the connections of the reptilian paleostriatum and its subdivisions. Then, studies with experimental tracing techniques of the afferent connections of the paleostriatum from the thalamus (e.g. Hall and Ebner, 1970) and cortex (Lohman and Mentink, 1972) appeared, later followed by studies on its efferent connections (e.g. Hoogland, 1977; Voneida and Sligar, 1979; Brauth and Kitt, 1980; Reiner et al., 1980; Ten Donkelaar and de Boer-van Huizen, 1981). These studies generally dealt with the paleostriatum as a whole, and not so much with its subdivisions.

Afferent Connections of the Striatum and the Nucleus accumbens in the Lizard Gekko gecko(Part 1 of 2)

The afferent connections of the striatum and the nucleus accumbens of the lizard Gekko gecko were studied with retrograde tracing by means of horseradish peroxidase and Fluoro-Gold and with anterograde tracing by means of Phaseolus vulgaris leukoagglutinin. The striatum receives projections from the cortex, the dorsal ventricular ridge, the lateral amygdaloid nucleus, the globus pallidus, the anterior peduncular nucleus, the ventral tegmental area and substantia nigra, the area ventral to the substantia nigra, and the dorsal thalamus. The nucleus accumbens is projected upon by the cortex, the diagonal band, the ventral pallidum, the lateral preoptic area, the ventral tegmental area, and the dorsal thalamus. The source of the cortical projection to the striatum and the nucleus accumbens is a longitudinal zone in the dorsal cortex that, rostrally in the hemisphere, is located medially and, more caudally, in its middle one third. The medial and rostrolateral areas of the dorsal ventricular ridge each project to the striatum in a vertical zone. The fibers from the caudolateral area of the ridge end in two oblique bands located parallel to the border between the dorsal ventricular ridge and the striatum. The pathways from the mesencephalic tegmentum to the striatum and the nucleus accumbens show a medial to lateral topography. This is similar to the situation in birds, but contrary to that in mammals in which these pathways are extensively interconnected. The specific sensory nuclei of the dorsal thalamus were found to project not only to the dorsal ventricular ridge, but also, and in a topographical fashion, to the striatum. The dorsomedial thalamic nucleus, which innervates the dorsal ventricular ridge, has additional projections to the striatum and the nucleus accumbens. This projection pattern is similar to that of the intralaminar thalamic nuclei of birds and mammals.