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The afferent connections of the main and accessory olfactory bulbs in the rat were examined by injecting horseradish peroxidase (HRP) into one or the other of these structures either by microelectrophoresis or by hydraulic pressure. Alternate sections were stained with newly developed HRP-procedures using either benzidine dihydrochloride (de Olmos and Heimer, '77) or tetramethyl-benzidine. Eighteen to twenty-four hours after unilateral HRP injections confined to the main olfactory bulb, a large number of HRP-labeled perikaria appeared in the following telencephalic structures on the ipsilateral side: All portions of the anterior olfactory nucleus (AON) except its external part, the lateral transitional field (LT) between AON and the paleocortex, the whole extent of the primary olfactory cortex (POC); the medial forebrain bundle area deep to the olfactory tubercle, the nucleus of the horizontal limb of the diagonal band (NHDB) and the nucleus of the lateral olfactory tract (NLOT). A moderate to small number of labeled cells, furthermore, were seen in the dorsal (DT) and medial (MT) transition fields, the ventral praecommissural hippocampus (tt2), the ventral superficial part of the nucleus of the vertical limb of the diagonal band (NVDB), the sublenticular part of the substantia innominata (SI), the anterior amygdaloid area, the posterolateral cortical amygdaloid nucleus (C2) and the transition region (28 L') between the olfactory cortex and the lateral entorhinal area proper. On the contralateral side a large number of labeled cells were found in all parts of the AON, with especially heavy labeling in its external part. A moderate number of labeled cells could also be detected in the lateral transition field (LT) and the NLOT. In the diencephalon and the brain stem a moderate number of HRP-labeled perikaria were observed in the dorsal, perifornical, and lateral hypothalamus, as well as in locus coeruleus and the dorsal and medial raphae nuclei. Following large HRP injections in the main olfactory bulb a moderate to small number of labeled cells were seen also in the posterior and premammillary hypothalamus and in field CA1 of the retrocommissural hippocampus on the ipsilateral side, as well as in POC on the contralateral side. It is possible, however, that the uptake of label took place in an undetected pool of HRP in the very rostal part of AON rather than in the olfactory bulb. HRP injections in the accessory olfactory bulb resulted in labeled neurons in the posterior ventro-lateral part of the bed nucleus of the stria terminalis, the nucleus of the accessory olfactory tract, the rostrodorsal portions of the medial amygdaloid nucleus, and the whole extent of the posteromedial cortical amygdaloid nucleus (C3) on the ipsilateral side. A few lightly labeled cells were seen also in the contralateral C3.

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We have examined the location of cholinergic and GABAergic neurons that project to the rat main olfactory bulb by combining choline acetyltransferase (ChAT) and glutamic acid decarboxylase (GAD) immunohistochemistry with retrograde fluorescent tracing. Since many of the projection neurons are located in subcortical basal forebrain structures, where the delineation of individual regions is difficult, particular care was taken to localize projection neurons with respect to such landmarks as the ventral pallidum (identified on the basis of GAD immunoreactivity), the diagonal band, and medial forebrain bundle. In addition, sections with fluorescent tracers or immunofluorescence were counterstained for Nissl substance in order to correlate tracer or immunopositive neurons with the cytoarchitecture of the basal forebrain. The majority of the cholinergic bulbopetal neurons are located in the medial half of the nucleus of the horizontal limb of the diagonal band (HDB), whereas only a few are located in its lateral half. A substantial number of cholinergic bulbopetal cells are also found in the sublenticular substantia innominata. A small number of cholinergic bulbopetal neurons, finally, are located in the ventrolateral portion of the nucleus of the vertical limb of the diagonal band. At the level of the crossing of the anterior commissure, approximately 17% of the bulbopetal neurons in the HDB are ChAT-positive. The noncholinergic bulbopetal cells are located mainly in the lateral half of the HDB. GAD-containing bulbopetal neurons are primarily located in the caudal part of the HDB, especially in its lateral part. About 30% of the bulbopetal projection neurons in the HDB are GAD-positive. A few GAD-positive bulbopetal cells, furthermore, are located in the ventral pallidum, anterior amygdaloid area, deep olfactory cortex, nucleus of the lateral olfactory tract, lateral hypothalamic area, and tuberomamillary nucleus. The topography of bulbopetal neurons was compared to other projection neurons in the HDB. After multiple injections of fluorescent tracer in the neocortex, retrogradely labeled neurons were concentrated in the most medial part of the HDB, while neurons projecting to the olfactory and entorhinal cortices were located in the ventral part of the HDB. These results show that the cells of the HDB can be divided into subpopulations based upon projection target as well as transmitter content. Furthermore, these subpopulations correspond, at least to a considerable extent, to areas that can be defined on cyto- and fibroarchitectural grounds.

The efferent connections of the rostral pole of the rat accumbens, where distinct core and shell subterritories can not be identified, were examined with the aid of the anterogradely transported plant lectin, Phaseolus vulgaris-leucoagglutinin (PHA-L), for comparison with the previously reported projection patterns of the accumbal core and shell. Injection sites and transported PHA-L were evaluated with the aid of reference to adjacent sections processed to display substance P or calbindin 28 kD immunoreactivities, i.e., markers that demonstrate the core and shell. Lateral parts of the rostral pole gave rise to a "core-like" projection system that involved the rostroventral globus pallidus, subcommissural ventral pallidum, entopeduncular nucleus and an adjacent part of the lateral hypothalamus, lateral ventral tegmental area, dorsal pars compacta, and structures in the lateral mesencephalic tegmentum and central grey. The medial part of the rostral pole gave rise to a "shell-like" innervation of the subcommissural ventral pallidum, lateral preoptic region, lateral hypothalamus, ventral tegmental area, dorsalmost pars compacta, retrorubral field, lateral midbrain tegmentum, and central grey. In contrast to the large numbers of axon varicosities observed through the entire length of lateral hypothalamus following shell injections, dense accumulations of axon collaterals and varicosities in hypothalamus were limited to the levels of origin of the stria medullaris bundle and entopeduncular nucleus and to the posterlateral region following medial injections. The medial part of the rostral pole contributed some projections to preoptic and sublenticular regions, but not to the bed nucleus of the stria terminalis. Noteworthy concentrations of calbindin immunoreactive cells observed in the lateral rostral pole correlate with the origin of the "basal ganglia-like" projection system, provoking the speculation that ventral striatal calbindin immunoreactive cells contribute principally to basal ganglia-like projections while cells lacking calbindin immunoreactivity contribute to the innervation of hypothalamus and midbrain tegmentum.

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The striatopallidal projection originating in the nucleus accumbens was investigated by using anterograde transport of PHA-L in combination with peptide immunohistochemistry in order to localize the injection sites and transported lectin with respect to neurochemically defined subterritories in the nucleus accumbens and subcommissural ventral pallidum. The results reported here supplement our previous observations, which indicated that the subcommissural ventral pallidum of the rat comprises two immunohistochemically defined subterritories (Zahm and Heimer, '88: J. Comp. Neurol., 272:516-535) which give rise to dichotomous downstream projection systems (Zahm, '89: Neuroscience, 30:33-50). The present data indicate that the neurotensin immunoreactivity-rich ventromedial district of ventral pallidum receives its accumbal input almost exclusively from the shell district of the nucleus accumbens. The accumbal core, alternatively, projects to the dorsolateral ventral pallidal subterritory that lacks appreciable neurotensin immunoreactivity and in many other respects more resembles the adjoining striatopallidal components of the caudate-putamen. In addition to direct topographic relationships in the frontal plane among the accumbal injection sites and ventral pallidal terminations, it was observed that more caudally placed core injections resulted in patches of striatopallidal terminations that were more caudally located in ventral pallidum. Shell injections, in contrast, produced columns of terminations that extended continuously from the rostralmost level that they appeared to the caudal end of ventromedial ventral pallidum. The accumbal shell, its exclusive projection to the ventromedial subterritory in the subcommissural ventral pallidum, and the previously reported, almost exclusive projection of that pallidal subdistrict to the mesencephalic ventral tegmental area are discussed in terms of a number of other neurochemical and hodological features that serve to distinguish them sufficiently to suggest that they represent a uniquely specialized part of the basal ganglia.