Axonal branching patterns of ventral pallidal neurons in the rat

Abstract

The ventral pallidum (VP) is a key component of the cortico-basal ganglia circuits that process motivational and emotional information, and also a crucial site for reward. Although the main targets of the two VP compartments, medial (VPm) and lateral (VPl) have already been established, the collateralization patterns of individual axons have not previously been investigated. Here we have fully traced eighty-four axons from VPm, VPl and the rostral extension of VP into the olfactory tubercle (VPr), using the anterograde tracer biotinylated dextran amine in the rat. Thirty to fifty percent of axons originating from VPm and VPr collateralized in the mediodorsal thalamic nucleus and lateral habenula, indicating a close association between the ventral basal ganglia-thalamo-cortical loop and the reward network at the single axon level. Additional collateralization of these axons in diverse components of the extended amygdala and corticopetal system supports a multisystem integration that may take place at the basal forebrain. Remarkably, we did not find evidence for a sharp segregation in the targets of axons arising from the two VP compartments, as VPl axons frequently collateralized in the caudal lateral hypothalamus and ventral tegmental area, the well-known targets of VPm, while VPm axons, in turn, also collateralized in typical VPl targets such as the subthalamic nucleus, substantia nigra pars compacta and reticulata, and retrorubral field. Nevertheless, VPl and VPm displayed collateralization patterns that paralleled those of dorsal pallidal components, confirming at the single axon level the parallel organization of functionally different basal ganglia loops.

Learning and Motivational Processes Contributing to Pavlovian–Instrumental Transfer and Their Neural Bases: Dopamine and Beyond

“…Retrograde labeling in the VPm produced by the two tracers is consistent with previous findings showing comparable numbers of neurons in the VP projection to the MD and VTA and, in addition, a small population of neurons that send collaterals to both structures (Zahm 2000;Tripathi et al 2013). Examination of c-Fos found a selective increase in c-Fos during specific transfer in MD-projecting neurons as well as in neurons innervating both MD and VTA compared to controls.…”

The Nucleus Accumbens: Mechanisms of Addiction across Drug Classes Reflect the Importance of Glutamate Homeostasis

“…This raises the possibility that D1 and D2 projections from the accumbens to the VP might give rise to distinct direct and indirect pathways through the VP (Sesack and Grace, 2010;Smith et al, 2013;Tripathi et al, 2013). However, recent work using transgenic D1-and D2-Cre mouse lines demonstrates that unlike the dorsal striatum, D1 and D2 afferents to the VP do not distinguish between direct or indirect basal ganglia pathways (Kupchik et al, 2015).…”

“…Efferents of the Nucleus Accumbens Shell. The medial NAshell projects to the ventromedial VP, which in turn projects to the medial part of the mediodorsal thalamus and VTA (Heimer et al, 1991;Tripathi et al, 2013). In addition, the medial NAshell projects to the lateral hypothalamus, a projection that may provide essential regulation of autonomous systems related to reward (Heimer et al, 1997).…”

The Direct and Indirect Pathways of the Nucleus Accumbens are not What You Think

“…Other than the classical D1-MSN-to-VM pathway, whether a neuron is part of a direct or indirect pathway is determined in the VP. Curiously, some 15% of VP cells project to both the VM and the thalamus (Tripathi et al, 2013), converging the direct and indirect pathway on the same neuron. Thus, our perspective of the reward system needs to be more nuanced than simply through the prism of the direct and indirect pathways.…”