Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat

Abstract

The paraventricular (PV) and paratenial (PT) nuclei are prominent cell groups of the midline thalamus. To our knowledge, only a single early report has examined PV projections and no previous study has comprehensively analyzed PT projections. By using the anterograde anatomical tracer, Phaseolus vulgaris leucoagglutinin, and the retrograde tracer, FluoroGold, we examined the efferent projections of PV and PT. We showed that the output of PV is virtually directed to a discrete set of limbic forebrain structures, including 'limbic' regions of the cortex. These include the infralimbic, prelimbic, dorsal agranular insular, and entorhinal cortices, the ventral subiculum of the hippocampus, dorsal tenia tecta, claustrum, lateral septum, dorsal striatum, nucleus accumbens (core and shell), olfactory tubercle, bed nucleus of stria terminalis (BST), medial, central, cortical, and basal nuclei of amygdala, and the suprachiasmatic, arcuate, and dorsomedial nuclei of the hypothalamus. The posterior PV distributes more heavily than the anterior PV to the dorsal striatum and to the central and basal nuclei of amygdala. PT projections significantly overlap with those of PV, with some important differences. PT distributes less heavily than PV to BST and to the amygdala, but much more densely to the medial prefrontal and entorhinal cortices and to the ventral subiculum of hippocampus. As described herein, PV/PT receive a vast array of afferents from the brainstem, hypothalamus, and limbic forebrain, related to arousal and attentive states of the animal, and would appear to channel that information to structures of the limbic forebrain in the selection of appropriate responses to changing environmental conditions. Depending on the specific complement of emotionally associated information reaching PV/PT at any one time, PV/PT would appear positioned, by actions on the limbic forebrain, to direct behavior toward a particular outcome over a range of outcomes.

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.…”

Different Fear States Engage Distinct Networks within the Intercalated Cell Clusters of the Amygdala

“…Within the amygdala, the basolateral complex (BLA) and the intercalated cell masses (ITCs) appear as two pivotal regions implicated in the acquisition and consolidation of extinction (Paré et al, 2004;Herry et al, 2010). The ITCs, in particular, may represent an important mediator of extinction because they (1) receive information about sensory stimuli from BLA and thalamus (Royer et al, 1999;Vertes and Hoover, 2008), (2) are under control of the mPFC (McDonald et al, 1996;Amano et al, 2010), and (3) give rise to inhibitory projections to the central medial nucleus (CEm) (Paré and Smith, 1993;Royer et al, 1999;Geracitano et al, 2007), the main output area of the amygdala for the expression of conditioned fear responses. Moreover, evidence that activity in ITC clusters is critical for fear extinction was obtained recently with the ablation of ITC neurons located in the intermediate capsule, which resulted in extinction retrieval deficits (Likhtik et al, 2008).…”

Medial Dorsal Hypothalamus Mediates the Inhibition of Reward Seeking after Extinction

“…PVT is critical for reinstatement of alcohol seeking (Dayas et al, 2008;Hamlin et al, 2009). PVT has extensive projections to basolateral amygdala (BLA), AcbSh, ventral subiculum, and PFC (Christie et al, 1987;Li and Kirouac, 2008;Vertes and Hoover, 2008), and projections from PVT to AcbSh are recruited during context-induced reinstatement ). Here we used complementary functional and neuroanatomical techniques, retrograde tract tracing, immunohistochemistry for the activity marker c-Fos, and pharmacological microinjections to identify the MDH afferents and efferents recruited during the expression of extinction of alcoholic beer seeking and to study the causal role of MDH in this extinction expression.…”