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Abstract:
The subiculum (Sub) of the hippocampal formation (HF) and the basal amygdala (Amy) control memory and other critical cognitive processes in part through the regulation of dopamine release from mesodiencephalic projecting neurons of the ventral tegmental area (VTA) (Phillips et al. 2003 Nsci Biobehav Rev 27:543-54; Belujon Grace 2011 ANYAS 1216:114-21). Models of the dopaminergic system proposed that HF regulates the activity of VTA through strong indirect pathways involving the striatum and lateral septum, without direct connections between HF and VTA (e.g., Lisman et al. 2005 Neuron 46:703-13). A prior tracing study in macaque monkeys showed that the central nucleus of Amy (CeA) projects to VTA (Amaral et al. 1981 J Nsci 1:1242-59); but evidence for a direct projection from other Amy nuclei, in particular the basal nucleus, is still missing. Here, we examined whether HF and amygdala nuclei other than CeA contribute direct monosynaptic projections to VTA. We analyzed the distribution of anterograde labeling produced in VTA with injections of biotin dextran amine and Phaseolus vulgaris leucoagglutinin in distinct architectonic regions in HF and Amy. Within HF, injections in the subiculum (Sub) produced dense anterograde labeling dispersed throughout VTA. Injections in the Ammon horns (CA1-3), dentate gyrus (DG) produced no labeling in VTA; and injections in entorhinal cortex (EC) produced labeling only in cases in which the injection contaminated the basal amygdala. Accordingly, baring CeA, injections in the amygdala produced labeling in VTA only for these injections that involved the magnocellular (Bmc), intermediate (Bi) or parvocellular (Bpc) parts of the basal nucleus, or the primate-specific paralaminar nucleus (PL). A comparison of the spatial distribution of anterogradely labeled fibers in VTA revealed a considerable overlap with only a subtle trend for two distinct labelling patterns; that is, either restricted to the rostral level of VTA, or dispersed throughout the rostrocaudal extent of VTA. While tenuous, the direct projections of Sub and basal Amy to VTA in the macaque monkey could produce direct regulation of dopaminergic release in parallel and/or independently of the classical indirect pathways involving ventral striatum and lateral septum.
