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Collateralization of projections from the paraventricular nucleus of the thalamus to the nucleus accumbens, bed nucleus of the stria terminalis, and central nucleus of the amygdala
Abstract
The paraventricular nucleus of the thalamus (PVT) is a midline thalamic nucleus with dense projections to the nucleus accumbens (NAc), dorsolateral region of the bed nucleus of the stria terminalis (BSTDL) and the lateral/capsular region of the central nucleus of the amygdala (CeL/CeC). Recent experimental evidence indicates that the PVT is involved in both appetitive and aversive behaviors. However, it is unknown if subgroups of neurons in the PVT innervate different subcortical targets or if the same neurons issue collaterals to multiple areas. To address this issue, we injected two different fluorescent retrograde tracers, cholera toxin subunit B conjugated to Alexa Fluor-488 or Alexa Fluor-594, into different pairs of the subcortical targets including different parts of the NAc (shell, core, dorsomedial shell, and ventromedial shell), BSTDL, and amygdala (basolateral amygdala and CeL/CeC). The results indicate a moderate to high level of collateralization of projections from neurons in the PVT to NAc, BSTDL, and CeL/CeC suggesting a potential importance of the PVT in simultaneously coordinating the activity of key regions of the brain involved in mediating emotional and motivational behaviors. We also observed a difference in the subcortical targets innervated by the anterior PVT (aPVT) and posterior PVT (pPVT) showing that more neurons in the aPVT innervate the dorsomedial part of the NAc shell, while more neurons in the pPVT innervate the ventromedial NAc shell, BSTDL, and CeL/CeC. This observation is suggestive of a potential functional difference between the aPVT and pPVT.
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“Given that the PVT projects to various reward-associated areas including the NAc, bed nucleus of the stria terminalis, and central amygdala through collateralized projections 10,14, mPFC->pPVT neurons are well-positioned to provide top-down control of brain networks.”
From A prefrontal–paraventricular thalamus circuit requires juvenile social experience to regulate adult sociability in mice (2020) · cites this paper as [14]
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“In contrast, the CeL and the BSTDL have been implicated in avoidance and defensive behaviors (Davis et al. 2010; LeDoux 2000) and pPVT projections to these areas may represent a means for the PVT to influence”
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“For example, the nucleus accumbens (a ventral striatal structure) and the amygdala share inter-connections via the paraventricular nucleus and the stria terminalis (e.g., Dong, Li, & Kirouac, 2017).”
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“Signals from these input neurons may propagate to several downstream targets, as PVT neurons have bifurcating axon projections throughout the extended amygdala, including the NAc (Dong et al., 2017).”
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“Next, to investigate the impact of disinhibition on stress circuits of the pPVT in vivo, we used an intersectional approach that allowed restricted expression of the genetically-encoded calcium sensor, GCaMP6s, in NAc-projecting pPVT neurons and assessed stress-evoked fluorescence changes with fiber photometry (Fig.”
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“Moreover, PVT neurons project to various reward-associated areas, including the VTA and NAc, which are key nodes of reward circuitry [93, 94].”
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“These regional differences between aPVT and pPVT are not surprising based on their differences in anatomical connectivity (Kirouac, 2015; Dong et al., 2017).”
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“Based on anatomic connectivity and functions, the PVT is divided into anterior (aPVT) and posterior (pPVT) portions along the rostrocaudal axis (Li and Kirouac, 2012; Li et al., 2014; Dong et al., 2017).”
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“Indeed, more than 50% of PVT neurons that project to the central amygdala (CeA) or BNST also send axon collaterals to the NAc [68,74].”
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“For retrograde tracing, 300 nl of cholera toxin B conjugated to Alexa Fluor 488 (CTb (488); Thermo Fisher, catalog #C34775) were microinjected to the right hemisphere NAc as previously (Dong et al., 2017; Park et al., 2018) at a rate of 100 nl/min and allowed 4 min for diffusion.”
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“Based on the findings that (1) the PVT-hypothalamus reciprocal projections are related to feeding behavior (Stratford and Wirtshafter, 2013) and (2) the PVT-prefrontal cortex circuit is responsible for decisionmaking (Pinto et al., 2003; Li and Kirouac, 2008; Dong et al., 2017), we propose that the PVT may represent a…”
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“The thalamus is composed of many nuclei; however, it has been demonstrated that it is the paraventricular nucleus of the thalamus (PVT) that provides the predominant glutamatergic projection to the NAc (Su and Bentivoglio, 1990; Bubser and Deutch, 1998; Pinto et al., 2003; Dong et al., 2017).”
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Projections from Infralimbic Cortex to Paraventricular Thalamus Mediate Fear Extinction Retrieval
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“Previous research has shown that unique PVT cell types can have opposing effects on behavior, as this structure contains many classes of neurons that can be distinguished by anatomical location (anterior versus posterior) 59 – 62 , function 9,63,64 , and gene expression 58,60 .”
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“27 This suggests a potential functional difference in visceral pain and anxiety processing between aPVT and pPVT. 38 The amygdala contains two primary nuclei: the basolateral amygdala (BLA) and the central amygdala (CeA).”
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How many brain regions are needed to elucidate the neural bases of fear and anxiety?
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A ventrolateral medulla-midline thalamic circuit for hypoglycemic feeding
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“Indeed, this is largely what occurs when the kappa opioid receptor is stimulated in the PVT itself or in two of its major projection regions, the BNST and nucleus accumbens shell (Dong et al., 2017).”
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“The results of the triple-injection experiments reported here are consistent with our previous study involving various combinations of the CTB injections where we found that many neurons in the PVT provide collateral innervation of the dmNAcSh, vmNAcSh, BSTDL and CeL (Dong et al. 2017).”
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“This is especially important since many of the neurons in the PVT that project to the NAcSh also send collaterals to the BSTDL and CeL (Dong et al., 2017).”
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“PVT contains a nearly pure population of glutamate cells [61], most of which innervate NAc shell [52,92,119], where they form synaptic connections with MSNs [119] and converge with DA afferents [10].”
BackgroundDissociable encoding of motivated behavior by parallel thalamo-striatal projections
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“However, to allow for pathway specificity and to avoid an effect on other areas because of collateralization (Dong et al., 2017), here we opted to administer clozapine-N-oxide (CNO; a DREADD ligand) locally at the areas of interest.”
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“While the relationship between dual mPFC-HC projecting PVT cells and these other projection targets is not known, it does speak to PVT as a unique node in integrating areas processing executive functions, motivated behaviors, salient cues, and memory (Dong et al. 2017; Zhu et al. 2018).”
BackgroundMethodInfluentialOrexin Modulation of VTA Dopamine Neuron Activity: Relevance to Schizophrenia
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“Of importance to this study is the PVT and its innervation of the NAc (Moga et al., 1995; Pinto et al., 2003; Kirouac, 2015; Dong et al., 2017).”
BackgroundCui, D., Guo, Y., Cao, W., Gao, W., Qiu, J., Su, L., Jiao, Q., & Lu, G. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00612 · Cited by 21
“These subnuclei have diverse functions physiologically and have been shown in disease models of BD to react differentially to pathological mechanisms (30, 31).”
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“injected bilaterally in the NAc shell with the PACAP receptor antagonists, PACAP (6-27) and PACAP (6-38) (20 and 200 ρmol/side).”
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“The PVT projects to many brain regions with important roles in stress and reward (22 – 24) and is thus poised to regulate behaviors related to stress and reward following salient early-life experiences.”
BackgroundTiming of Morphine Administration Differentially Alters Paraventricular Thalamic Neuron Activity
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“Additionally, the PVT projects to several regions of the greater reward circuit, including the nucleus accumbens, amygdala, and medial prefrontal cortex (Li and Kirouac, 2008; Kirouac, 2015; Dong et al., 2017).”
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“…in its unconjugated form and when conjugated with horseradish peroxidase, for the anterograde, retrograde, and transganglionic tracing of neural pathways (Hirakawa et al., 1992; Ciriello and Caverson, 2016; Dong et al., 2017; Wang et al., 2018; Cui et al., 2019; Han et al., 2019; Ma et al., 2020).”
BackgroundInfluentialInternalizing–externalizing comorbidity and regional brain volumes in the ABCD study
Schettini, E., Wilson, S., & Beauchaine, T. P. (2021) · Development and Psychopathology · doi:10.1017/s0954579421000560 · Cited by 21
“These subcortical regions share functional interconnections via the paraventricular nucleus and the stria terminalis (e.g., Dong, Li, & Kirouac, 2017).”
BackgroundBu, X., Liu, C., & Fu, B. (2022) · Ibrain · doi:10.1002/ibra.12034 · Cited by 16
“27 Furthermore, it was found that aPVT has fiber projections to pPVT, but no projections from pPVT to aPVT were found, suggesting that information transfer within the PVT may be unidirectional.”
Curtis, G. R., Gargiulo, A. T., Carpenter, B. A., Pirino, B. E., Hawks, A., Coleman, S. A., Syed, N., Gupta, A., & Barson, J. R. (2022) · Addiction Neuroscience · doi:10.1016/j.addicn.2022.100058 · Cited by 16
Li, S. H., Li, S., & Kirouac, G. J. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.11.033 · Cited by 15
“…that includes the shell of the nucleus accumbens (NAcSh), dorsolateral bed nucleus of the stria terminalis (BSTDL) and lateral central nucleus of the amygdala (CeL) (Moga et al., 1995; Li and Kirouac, 2008; Parsons et al., 2007; Dong et al., 2017; Vertes and Hoover, 2008; Li et al., 2021).”
BackgroundMethodResultInfluentialSelf-citationKirouac, G. J. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105989 · Cited by 16
Self-citationDai, L., Mai, J.-W., Deng, J., Chen, L., Fan, H.-T., Zhang, W.-L., Xin, W., Feng, X., Xu, T. S., & Luo, D. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106699 · Cited by 14
“Functionally, researches suggested that the different neural circuits involving PVT subregions (PVA and PVP) may mediate distinct biological functions (Dong et al., 2017; Moga and Moore, 1997).”
BackgroundThe neurobiology of abstinence-induced reward-seeking in males and females
Alonso‐Caraballo, Y., Guha, S. K., & Chartoff, E. H. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173088 · Cited by 15
“This anatomical distinction is important, although not fully understood, because the dorsal and ventral subregions of the NAcSh can have opposing effects on motivated behavior (Al-Hasani et al., 2015; Marchant et al., 2009; Millan et al., 2017).”
MethodInfluentialSex differences in activation of extra-hypothalamic forebrain areas during hedonic eating
Parsons, W. S., Greiner, E. M., Buczek, L., Migliaccio, J., Corbett, E., Madden, A. M. K., & Petrovich, G. D. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02580-0 · Cited by 15
“This is intriguing, because the CEA was the only area analyzed in the current study where Fos induction was positively correlated with consumption at test, and because of the connectional network between the PVT, ACB and CEA (Dong et al. 2017).”
BackgroundMethodMindaye, S. A., Chen, W.-H., Lin, S.-C., Chen, Y.-C., Abdelaziz, M. A., Tzeng, Y.-S., Shih, A. C.-C., Chen, S.-Y., Yang, S., & Chen, C. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114946 · Cited by 13
McDevitt, D. S., Wade, Q. W., McKendrick, G., Nelsen, J. L., Starostina, M., Tran, N. A., Blendy, J. A., & Graziane, N. (2024) · eNeuro · doi:10.1523/eneuro.0524-23.2024 · Cited by 12
“However, this is unlikely as PVT neurons that project to the NAc core are less numerous than those to the NAcSh (Dong et al., 2017) and our trypan blue procedure showed minimal NAc core staining.”
BackgroundFiedler, D., Pape, H., & Lange, M. D. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110338 · Cited by 11
Kirouac, G. J., Li, S., & Li, S. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02534-6 · Cited by 12
“…nucleus of the stria terminalis (BSTDL), lateral central nucleus of the amygdala (CeL) (Moga et al. 1995; Li and Kirouac 2008; Parsons et al. 2007; Dong et al. 2017; Vertes and Hoover 2008; Li et al. 2021) through which the PVT has been shown to regulate a behavior (Choi et al. 2019; Choi and…”
BackgroundInfluentialSelf-citationFunctional properties of corticothalamic circuits targeting paraventricular thalamic neurons
Aquino-Miranda, G., Jalloul, D., Zhang, X. O., Li, S., Kirouac, G. J., Beierlein, M., & Monte, F. H. D. (2024) · Neuron · doi:10.1016/j.neuron.2024.10.010 · Cited by 12
Self-citationJi, R., Cui, M., Zhou, D., Pan, X., Xie, Y., Wu, X., Liang, X., Zhang, H., & Song, W. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.115205 · Cited by 10
Li, J., Gao, P., Zhang, S., Lin, X., Chen, J., Zhang, S., Jiao, Y., Yu, W., Xia, X., & Yang, L. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14367 · Cited by 10
Petersen, D., Raudales, R., Silva, A. K., Kellendonk, C., & Canetta, S. (2024) · eNeuro · doi:10.1523/eneuro.0284-24.2024 · Cited by 11
“…while the dual virus approach targets midline and mediodorsal thalamic projections to the mPFC, some of these neurons, especially in the paraventricular, have been shown to possess collaterals to the nucleus accumbens, bed nucleus of the stria terminalis, and the amygdala (Dong et al., 2017).”
BackgroundKooiker, C. L., Hardy, M., Birnie, M. T., Chen, Y., de Carvalho, G., Floriou‐Servou, A., Ding, Q., Thiagarajan, N., Tetzlaff, M. R., Smith, A., et al. (2026) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2026.100840 · Cited by 10
Rat Paraventricular Neurons Encode Predictive and Incentive Information of Reward Cues
Munkhzaya, U., Chinzorig, C., Matsumoto, J., Nishimaru, H., Ono, T., & Nishijo, H. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.565002 · Cited by 8
Hill-Bowen, L. D., Flannery, J. S., & Poudel, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1945-19.2019 · Cited by 8
“Consistent with this observation, a greater number of neurons in the pPVT (vs aPVT) send collateral efferents to the lateral and central amygdala, nuclei commonly implicated in avoidance behaviors (Dong et al., 2017).”
BackgroundGargiulo, A. T., Badve, P. S., Curtis, G. R., Prino, B. E., & Barson, J. R. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06160-2 · Cited by 7
Neuropeptide S Encodes Stimulus Salience in the Paraventricular Thalamus
Garau, C., Liu, X., Calò, G., Schulz, S., & Reinscheid, R. K. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.013 · Cited by 8
“For example, no c-fos staining was observed in the central amygdala or bed nucleus of the stria terminalis (Dong et al., 2017; Li et al., 2021).”
InfluentialDeng, Q., Zhang, S.-Q., Yang, P., Dong, W., Wang, J., Chen, J., Wang, F., & Long, L. (2022) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14046 · Cited by 7
Stress peptides sensitize fear circuitry to promote passive coping
Pliota, P., Groessl, F., Griessner, J., Pasieka, M., Deussing, J. M., & Haubensak, W. E. (2018) · doi:10.26226/morressier.5b31ec542afeeb001345b89c · Cited by 8
A glutamatergic brain neural circuit is critical for modulating trigeminal neuropathic pain
Liu, S., Crawford, J. A., Maltezos, H., Sun, Y., Tao, R., & Tao, F. (2025) · Pain · doi:10.1097/j.pain.0000000000003647 · Cited by 7
Activation patterns in male and female forebrain circuitries during food consumption under novelty
Greiner, E., Witt, M. E., Moran, S. J., & Petrovich, G. D. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02742-8 · Cited by 8
“This paradigm design allowed us to separately analyze the effects of sex, context, and food type on consumption and neural activation.”
Mitochondrial dysfunction in bipolar disorder
Kato, T. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-821398-8.00014-x · Cited by 7
Stratilov, V. A., Vetrovoy, O. V., Potapova, S., & Tyulkova, E. I. (2024) · Neuroendocrinology · doi:10.1159/000536214 · Cited by 6
“…the decreased α 7 nAChR-positive innervation was an outcome of decreased protein levels in the structures that spread excitatory glutamate inputs into the NAc, we assessed the levels of α 7 subunits in the PFC, HPC, AMG, and thalamic PVN, which also spread minor projections into the NAc [34, 35].”
MethodReiley, H. B., McCoy, A. M., Boley, A. M., Yang, O. J., Belle, N. I., & Lodge, D. J. (2025) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaf034 · Cited by 5
“…to influence VTA dopamine neuron population activity, either may be a viable target for alleviating symptoms of psychosis in PTSD. 20,21,30,33,34,37 38-41 Previous work from our laboratory has demonstrated that glutamatergic projections from the vHipp and PVT converge onto individual medium spiny…”
Refocusing Neuroscience: Moving Away from Mental Categories and Toward Complex BehaviorsPreprint
Pessoa, L., Medina, L. M., & Desfilis, E. (2021) · OSF Preprints (OSF Preprints) · doi:10.31219/osf.io/8cmhg · Cited by 6
Rivera-Irizarry, J. K., Hámor, P. U., Rowson, S. A., Asfouri, J. J., Liu, D., Zallar, L. J., Garcia, A. F., Skelly, M. J., & Pleil, K. E. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.03.547570 · Cited by 6
Metadata
- Authors
- Dong, X., Li, S., & Kirouac, G. J.
- Affiliations
- University of Manitoba (CA)
- Corresponding author
- Kirouac, Gilbert J.
- Venue
- Brain Structure and Function
- Published
- 2017-05-20
- Volume
- 222
- Issue
- 9
- Pages
- 3927-3943
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- OpenAlex
- W2616069238
- Cited by
- 143
- References
- 61
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 17 · 2023: 14 · 2022: 21 · 2021: 26 · 2020: 19 · 2019: 8 · 2018: 10 · 2017: 3
- FWCI
- 6.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Structure and Function (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Institute of Neurosciences, Mental Health and Addiction (MOP89758)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- paraventricular thalamus, collateral projections, nucleus accumbens, bed nucleus of the stria terminalis, central amygdala, subcortical projections, cholera toxin B subunit, retrograde tracing
- MeSH terms
- Animals, Brain Mapping, Cholera Toxin, Functional Laterality, Male, Neural Pathways, Nucleus Accumbens, Phosphopyruvate Hydratase, Septal Nuclei, Rats, Sprague-Dawley, Midline Thalamic Nuclei, Rats
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