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Neuroscience and Biobehavioral Reviews 56 (2015) 315–329

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Neuroscience and Biobehavioral Reviews 56 (2015) 315–329 Neuroscience and Biobehavioral Reviews 56 (2015) 315–329 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews jou rnal homepage: www.elsevier.com/locate/neubiorev Review Placing the paraventricular nucleus of the thalamus within the brain circuits that control behavior ∗ Gilbert J. Kirouac Departments of Oral Biology and Psychiatry, Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba, Canada a r t i c l e i n f o a b s t r a c t Article history: This article reviews the anatomical connections of the paraventricular nucleus of the thalamus (PVT) Received 6 January 2015 and discusses some of the connections by which the PVT could influence behavior. The PVT receives Received in revised form 29 July 2015 neurochemically diverse projections from the brainstem and hypothalamus with an especially strong Accepted 4 August 2015 innervation from peptide producing neurons. Anatomical evidence is also presented which suggests that Available online 7 August 2015 the PVT relays information from neurons involved in visceral or homeostatic functions. In turn, the PVT is a major source of projections to the nucleus accumbens, the bed nucleus of the stria terminalis and the Keywords: central nucleus of the amygdala as well as the cortical areas associated with these subcortical regions. Paraventricular nucleus of the thalamus Motivation The PVT is activated by conditions and cues that produce states of arousal including those with appetitive Emotions or aversive emotional valences. The paper focuses on the potential contribution of the PVT to circadian Arousal rhythms, fear, anxiety, food intake and drug-seeking. The information in this paper highlights the poten- Nucleus accumbens tial importance of the PVT as being a component of the brain circuits that regulate reward and defensive Prefrontal cortex behavior with the hope of generating more research in this relatively understudied region of the brain. Amygdala © 2015 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND Bed nucleus of the stria terminalis license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Drug addiction Fear Anxiety Food intake Circadian rhythms Contents 1. Introduction . 316 2. Midline and intralaminar nuclei of the thalamus . 316 3. Types of neurons found in the PVT . 317 4. Sources of afferents to the PVT . 317 4.1. Brainstem . 317 4.2. Diencephalon . 317 4.3. Telencephalon. .318 4.4. Dense innervation of the PVT by peptidergic fibers . 318 4.5. Summary of afferents and functional considerations . 319 5. Areas innervated by the PVT . 319 5.1. Nucleus accumbens and the striatum . 320 5.2. Extended amygdala . 322 5.3. Cortical areas . 322 5.4. Other areas . 323 5.5. Summary of efferents and functional circuits . 323 6. Summary . 323 Acknowledgements . 324 References . 325 ∗ Correspondence to: Department of Oral Biology, Faculty of Health Sciences, 780 Bannatyne Avenue, Winnipeg, Manitoba R3E 0W2, Canada. E-mail address: [email protected] http://dx.doi.org/10.1016/j.neubiorev.2015.08.005 0149-7634/© 2015 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 316 G.J. Kirouac / Neuroscience and Biobehavioral Reviews 56 (2015) 315–329 1. Introduction There is growing interest in the potential contribution of the paraventricular nucleus of the thalamus (PVT) in the modulation of behavior. Much of this attention has been driven by the recog- nition that the PVT is a major source of input to the nucleus accumbens (NAc), an area of the ventral striatum known to medi- ate motivation and reward. Even so, the numbers of studies that have focused on the other major sources of inputs to the NAc (pre- frontal cortex, basolateral amygdala, and hippocampal subiculum) far exceed those on the PVT. This may be due to the belief that the PVT and other thalamic midline nuclei are involved in gener- alized arousal (Groenewegen and Berendse, 1994), which is often considered a nonspecific determinant of behavior. The discovery of potent arousal peptides called orexins (hypocretins) and the subsequent interest in the contribution of arousal mechanisms to behavior (Boutrel et al., 2010; Mahler et al., 2014; Sakurai, 2014) have likely contributed to the recent surge of interest in the PVT (Kelley et al., 2005; Kirouac et al., 2005). The purpose of the present paper is to review and evaluate what is known about the anatomy of the PVT and to integrate this information into a functional frame- work to help guide future studies. The paper focuses on anatomical studies that have been done in rodents and readers interested in the anatomical connections of the PVT in primates should refer to studies done in that species (Hsu and Price, 2007, 2009) while those interested in a discussion on the differences between rodents and primates are referred to other reviews (Colavito et al., 2014; Hsu et al., 2014). The paper deliberately focuses on the more robust anatomical connections of the PVT since these are most likely to be involved in mediating observable behavioral changes in the labora- tory. As a final point, generalizations about the pattern of efferent and afferent connections of the PVT are made with the intent of providing insights on how the PVT fits within a complex network of neuronal systems involved in behavior. 2. Midline and intralaminar nuclei of the thalamus The PVT is a member of the midline and intralaminar group of thalamic nuclei originally hypothesized to function as a thala- mocortical arousal system (Edwards and de Olmos, 1976; Royce et al., 1989; Vertes and Martin, 1988). As shown in Fig. 1, the shape of the PVT along with its position relative to other midline and intralaminar nuclei varies across the anterior-posterior extent of the thalamus. The PVT is the dorsal most member of the midline group that includes the intermediodorsal and centromedial nuclei in addition to the PVT (Bentivoglio et al., 1991; Groenewegen and Berendse, 1994). The midline group shares common features in that these nuclei receive strong peptidergic innervation (Freedman and Fig. 1. Drawing of the nuclei and fiber bundles found in the dorsal midline tha- Cassell, 1994b; Kirouac et al., 2005; Lee et al., 2014) and that they lamus at the anterior (−1.32 mm), middle (−2.76 mm), and posterior (−3.48 mm) innervate the prefrontal cortex and ventromedial striatal regions levels relative to bregma. AM, anteromedial thalamic nucleus; CM, central medial thalamic nucleus; fr, fasciculus retroflexus; Hb, habenular; IMD, intermediodor- associated with these cortical areas (Groenewegen and Berendse, sal thalamic nucleus; MD, mediodorsal thalamic nucleus; PC, paracentral thalamic 1994). The anterior aspect of the PVT (aPVT) is bordered later- nucleus; PT, paratenial thalamic nucleus; PVT, paraventricular thalamic nucleus; ally by the paratenial nucleus whereas the mid to posterior aspect sm, stria medullaris of the thalamus. The figure was produced by modifying images of the PVT (pPVT) is bordered by the mediodorsal nucleus. The from a stereotaxic atlas of the rat brain (Paxinos and Watson, 2009). rhomboid and reuniens nuclei are also distinctive midline thala- mic nuclei found ventral to the centromedial nucleus. The earlier view of the midline and intralaminar nuclei having a general- 1990). As an example of this, the parafascicular nucleus innervates ized and nonspecific arousal influence on the cerebral cortex is the sensorimotor cortex and the lateral regions of the dorsal stria- no longer supported. This is in part due to anatomical studies tum which together form a circuit that regulates limb movements showing that individual members of the midline and intralaminar (Alexander et al., 1990; Groenewegen and Berendse, 1994; Van der nuclei innervate unique and circumscribed regions of the cortex Werf et al., 2002). This type of anatomical arrangement suggests (Groenewegen and Berendse, 1994; Van der Werf et al., 2002). that individual midline and intralaminar nuclei are part of special- It is especially important to appreciate that specialized cortical ized corticostriatal and corticolimbic systems. Indeed, investigators areas and their striatal targets form functional circuits that regulate now emphasize how different members of midline and intralam- specific components of movement and behavior (Alexander et al., inar group of nuclei regulate brain mechanisms associated with G.J. Kirouac / Neuroscience and Biobehavioral Reviews 56 (2015) 315–329 317 specific functions related to either attention, movement, cognition 1998). The PVT contains a relatively high concentration of fibers or emotions (for more details of this subject, see Groenewegen and immunoreactive to tyrosine hydroxylase, the enzyme involved in Berendse, 1994; Kimura et al., 2004; McHaffie et al., 2005; Smith the synthesis of DA and norepinephrine, and phenylethanolamine et al., 2004; Van der Werf et al., 2002; Vertes, 2006). N-methyltransferase (PNMT), the enzyme involved in the synthe- sis of epinephrine (Otake and Ruggiero, 1995). In addition, the PVT contains fibers immunoreactive for serotonin (Otake and Ruggiero, 3. Types of neurons found in the PVT 1995). The source of DA fibers in the PVT is from neurons in the hypothalamus.
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