Interconnected Parallel Circuits between Rat Nucleus Accumbens and Thalamus Revealed by Retrograde Transynaptic Transport of Pseudorabies Virus

Abstract

One of the primary outputs of the nucleus accumbens is directed to the mediodorsal thalamic nucleus (MD) via its projections to the ventral pallidum (VP), with the core and shell regions of the accumbens projecting to the lateral and medial aspects of the VP, respectively. In this study, the multisynaptic organization of nucleus accumbens projections was assessed using intracerebral injections of an attenuated strain of pseudorabies virus, a neurotropic ␣ herpesvirus that replicates in synaptically linked neurons. Injection of pseudorabies virus into different regions of the MD or reticular thalamic nucleus (RTN) produced retrograde transynaptic infections that revealed multisynaptic interactions between these areas and the basal forebrain. Immunohistochemical localization of viral antigen at short postinoculation intervals confirmed that the medial MD (m-MD) receives direct projections from the medial VP, rostral RTN, and other regions previously shown to project to this region of the thalamus. At longer survival intervals, injections confined to the m-MD resulted in transynaptic infection of neurons in the accumbens shell but not in the core. Injections that also included the central segment of the MD produced retrograde infection of neurons in the lateral VP and the polymorph (pallidal) region of the olfactory tubercle (OT) and transynaptic infection of a small number of neurons in the rostral accumbens core. Injections in the lateral MD resulted in retrograde infection in the globus pallidus (GP) and in transynaptic infection in the caudateputamen. Viral injections into the rostroventral pole of the RTN infected neurons in the medial and lateral VP and at longer postinoculation intervals, led to transynaptic infection of scattered neurons in the shell and core. Injection of virus into the intermediate RTN resulted in infection of medial VP neurons and second-order infection of neurons in the accumbens shell. Injections in the caudal RTN or the lateral MD resulted in direct retrograde labeling of cells within the GP and transynaptic infection of neurons in the caudate-putamen. These results indicate that the main output of VP neurons receiving inputs from the shell of the accumbens is heavily directed to the m-MD, whereas a small number of core neurons appear to influence the central MD via the lateral VP. Further segregation in the flow of information to the MD is apparent in the organization of VP and GP projections to subdivisions of the RTN that give rise to MD afferents. Collectively, these data provide a morphological basis for the control of the thalamocortical system by ventral striatal regions, in which parallel connections to the RTN may exert control over activity states of cortical regions.

Cocaine-Induced Synaptic Alterations in Thalamus to Nucleus Accumbens Projection

“…A major source of glutamatergic projection to the NAc is the PVT (Berendse and Groenewegen, 1990;O'Donnell et al, 1997;Van der Werf et al, 2002;Smith et al, 2004;Vertes and Hoover, 2008). Our current results reveal that synaptic transmission in PVT neurons projecting to the NAc is essential for acquisition of cocaine self-administration but not for incubation of cocaine craving after cocaine withdrawal.…”

“…One of the less-examined major projections is from the paraventricular nucleus of the thalamus (PVT), which, as a subnucleus of the thalamus, lies on the midline just ventral to the third ventricle (Van der Werf et al, 2002;Smith et al, 2004). The PVT projection often converges with other excitatory inputs or midbrain-originated dopaminergic terminals onto the same NAc medium spiny neurons (MSNs; Berendse and Groenewegen, 1990;O'Donnell et al, 1997;Otake and Nakamura, 1998;Pinto et al, 2003;Vertes and Hoover, 2008). This anatomical setup allows the PVT-to-NAc projection to either activate NAc MSNs directly or interact with other inputs.…”

Reduced Gray Matter Volume of Auditory Cortical and Subcortical Areas in Congenitally Deaf Adolescents: A Voxel-Based Morphometric Study

“…The serotonergic axons of the nucleus accumbens stimulate the thalamic reticular nucleus, and serotonin excites the GABAergic neurons of the thalamic reticular nucleus (34). An interconnected circuit also exists between the thalamic reticular nucleus and the nucleus accumbens, with the nucleus accumbens subsequently influencing inhibitory gating on the thalamocortical relay (35). The input of the thalamic reticular nucleus inhibits the neurons of the medial geniculate nucleus (36).…”

Transneuronal Labeling of a Nociceptive Pathway, the Spino-(Trigemino-)Parabrachio-Amygdaloid, in the Rat

“…This virus retrogradely infects synaptically connected neurons in the CNS after injection into various peripheral organs (Card and Enquist, 1994;Loewy, 1995) and, as found more recently, after direct injection in the CNS (Kaufman et al, 1996;O'Donnell et al, 1997). The latter studies, however, revealed problems specific to CNS injection; in particular, it has not been possible to determine the extent of the injection site histologically.…”