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Projections of the Paraventricular and Paratenial Nuclei of the Dorsal Midline Thalamus in the Rat

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Projections of the Paraventricular and Paratenial Nuclei of the Dorsal Midline Thalamus in the Rat THE JOURNAL OF COMPARATIVE NEUROLOGY 508:212–237 (2008) Projections of the Paraventricular and Paratenial Nuclei of the Dorsal Midline Thalamus in the Rat ROBERT P. VERTES* AND WALTER B. HOOVER Center for Complex Systems and Brain Sciences, Florida Atlantic University, Boca Raton, Florida 33431 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 antero- grade 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. J. Comp. Neurol. 508: 212–237, 2008. © 2008 Wiley-Liss, Inc. Indexing terms: medial prefrontal cortex; subiculum of hippocampus; nucleus accumbens; bed nucleus of stria terminalis; central and basal nuclei of amygdala The paraventricular and paratenial nuclei are promi- global effects on the cortical mantle (Bentivoglio et al., nent cell groups of the midline thalamus (Swanson, 1998; 1991; Groenewegen and Berendse, 1994). The notion, how- Van der Werf et al., 2002). The paraventricular nucleus ever, of the midline thalamus as ‘nonspecific’ has been (PV) lies dorsally on the midline directly below the third revised based on the subsequent anatomical demonstra- ventricle and extends rostrocaudally virtually throughout the thalamus. The paratenial nucleus (PT) borders PV laterally and overlaps with approximately the rostral one- Grant sponsor: National Institute of Mental Health; Grant numbers: third of PV. MH42900, MH63519. Based on the early demonstration that low-frequency *Correspondence to: Dr. Robert P. Vertes, Center for Complex Systems stimulation of the midline and intralaminar nuclei of the and Brain Sciences, Florida Atlantic University, Boca Raton, FL 33431. E-mail: [email protected] thalamus produced slow synchronous activity over wide- Received 29 August 2007; Revised 20 December 2007; Accepted 10 Jan- spread regions of the cortex (recruiting responses) (Demp- uary 2008 sey and Morrison, 1942), the midline thalamus was DOI 10.1002/cne.21679 viewed as ‘nonspecific’ thalamus, exerting nonspecific or Published online in Wiley InterScience (www.interscience.wiley.com). © 2008 WILEY-LISS, INC. The Journal of Comparative Neurology EFFERENTS OF PV AND PT NUCLEI 213 tion that nuclei of the midline thalamus do not project (mPFC) and ACC were themselves directly connected widely throughout the neocortex, but rather selectively to (mPFC to ACC). With respect to the paraventricular nu- specific regions of cortex, primarily those of the prefrontal cleus, PV distributes to the prelimbic cortex (of mPFC) cortex (Berendse and Groenewegen, 1991; Van der Werf et and to the medial shell region of ACC, and PL, in turn, al., 2002; Groenewegen and Witter, 2004; Vertes, 2006). In projects to the shell of ACC (Berendse and Groenewegen, addition, recent reports have shown that stimulation of 1990, 1991; Berendse et al., 1992). individual nuclei of the midline thalamus produce selec- Undoubtedly owing to the early emphasis on PV projec- tive effects on their cortical targets—as opposed to wide- tions to the ventral striatum and to mPFC, subsequent spread actions throughout the cortex (Dolleman-Van der reports largely focused on these target sites. Using dual Weel et al., 1997; Bertram and Zhang, 1999; Kung and retrograde labeling techniques, Otake and Nakamura Shyu, 2002; Zhang and Bertram, 2002; Viana Di Prisco (1998) reported that of the nuclei of the midline thalamus, and Vertes, 2006). PV contained the largest percentage of cells with collat- In a series of reports, Groenewegen and colleagues (Be- eral projections to ACC and mPFC. In like manner, Bub- rendse and Groenewegen, 1990, 1991; Berendse et al., ser and Deutch (1998) showed that Ϸ15% of PV cells 1992; Groenewegen et al., 1999) showed that major tar- distribute via collaterals to the medial shell of ACC and PL, gets of midline thalamic nuclei were the prefrontal cortex while Pinto et al. (2003) demonstrated that PV fibers termi- and ventral striatum (nucleus accumbens, ACC), and fur- nate in close apposition to dopaminergic (DA) terminals in ther that recipient zones in the medial prefrontal cortex nucleus accumbens, but not to DA terminals in the mPFC. Abbreviations AA Anterior amygdaloid area MFB Medial forebrain bundle ac Anterior commissure MG Medial geniculate nucleus of thalamus AC Anterior cingulate cortex MH Medial habenula ACC,c,s Nucleus accumbens, core and shell divisions MO Medial orbital cortex AGm Medial agranular (frontal) cortex mPFC Medial prefrontal cortex AGl Lateral agranular (frontal) cortex MPO Medial preoptic area AH Anterior nucleus of hypothalamus MPN Medial preoptic nucleus AI,d,p,v Agranular insular cortex, dorsal, posterior, ventral divi- MRF Mesencephalic reticular formation sions MS Medial septum AM Anteromedial nucleus of thalamus mt Mammillothalamic tract AON Anterior olfactory nucleus OC Occipital cortex AV Anteroventral nucleus of thalamus OT Olfactory tubercle BLA Basolateral nucleus of amygdala PAp Posterior parietal cortex BMA Basomedial nucleus of amygdala PC Paracentral nucleus of thalamus BST Bed nucleus of stria terminalis PFC Prefrontal cortex CA1,3 Field CA1 and CA3 of Ammon’s horn PH Posterior nucleus of hypothalamus cc Corpus callosum PHA-L Phaseolus vulgaris-leucoagglutinin CEA,c,l,m Central nucleus of amygdala, capsular, lateral, and me- PIR Piriform cortex dial divisions PL Prelimbic cortex CL Central lateral nucleus of the thalamus PO Posterior nucleus of thalamus CLA Claustrum PRC Perirhinal cortex CM Central medial nucleus of thalamus PT Paratenial nucleus of thalamus COA,a,p Cortical nucleus of amygdala, anterior, posterior divisions PV,a,p Paraventricular nucleus of thalamus, anterior and poste- CP Caudate-putamen rior divisions DBh Nucleus of diagonal band, horizontal limb RE Nucleus reuniens of thalamus DMh Dorsomedial nucleus of hypothalamus RH Rhomboid nucleus of thalamus EC,l Entorhinal cortex, lateral division RN Red nucleus ECT Ectorhinal cortex RSC Retrosplenial cortex EN Endopiriform nucleus RT Reticular nucleus of thalamus fa Forceps of the corpus callosum SC Superior colliculus FG Fluorogold SCN Suprachiasmatic nucleus FI Fimbria of hippocampus SI Substantia innominata FP,l,m Frontal polar cortex, lateral, medial divisions sm Stria medullaris FS Fundus of striatum SM Submedial nucleus of thalamus GI Granular insular cortex SNr Substantia nigra, pars reticulata GP Globus pallidus SPZ Subparaventricular zone of hypothalamus HF Hippocampal formation SSI Primary somatosensory cortex IAM Interanteromedial nucleus of thalamus SSII Secondary somatosensory cortex IL Infralimbic cortex st Stria terminalis IMD Intermediodorsal nucleus of thalamus SUB,v Subiculum, ventral division IP Interpeduncular nucleus SUM Supramammillary nucleus LA Lateral nucleus of amygdala TE Temporal cortex LD Lateral dorsal nucleus of thalamus TT,d,v Tenia tecta, dorsal and ventral divisions LH Lateral habenula V3 Third ventricle LHy Lateral hypothalamus VAL Ventral anterior nucleus of thalamus LO Lateral orbital cortex VB Ventral basal nucleus of thalamus LP Lateral posterior nucleus of thalamus VL Lateral ventricle LPO Lateral preoptic area VLO Ventrolateral orbital cortex LS Lateral septum VM Ventral medial nucleus of thalamus MA Magnocellular preoptic nucleus VO Ventral orbital cortex MD Mediodorsal nucleus of thalamus VTA Ventral tegmental area MEA Medial nucleus of the amygdala ZI Zona incerta The Journal of Comparative Neurology 214 R.P. VERTES AND W.B. HOOVER To our knowledge, only a single report (Moga et al., ventral striatum, lateral septum, bed nucleus of stria ter- 1995) has examined the general distribution of PV projec- minalis, and to most of the amygdala, with a concentra- tions “with special emphasis on the projections to the tion in the central and basal nuclei of the amygdala. hypothalamus and
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