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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The PVT projects to various reward-associated areas including the NAc, bed nucleus of the stria terminalis, and central amygdala through collateralized projections.
“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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Projections from Infralimbic Cortex to Paraventricular Thalamus Mediate Fear Extinction Retrieval
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An opioid-gated thalamoaccumbal circuit for the suppression of reward seeking in mice
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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 .”
BackgroundPaniccia, J. E., Vollmer, K. M., Green, L. M., Grant, R. I., Winston, K. T., Buchmaier, S., Westphal, A. M., Clarke, R. E., Doncheck, E. M., Bordieanu, B., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.024 · Cited by 42 · see citing works
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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).”
The nucleus accumbens shell: a neural hub at the interface of homeostatic and hedonic feeding
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The paraventricular thalamus input to central amygdala controls depression-related behaviors
Zhao, D., Liu, C., Cui, M., Liu, J., Meng, F., Lian, H., Wang, D., Hu, F., Liu, D., & Li, C. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113744 · Cited by 37 · see citing works
Extinction blunts paraventricular thalamic contributions to heroin relapse
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Thalamo-Nucleus Accumbens Projections in Motivated Behaviors and Addiction
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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).”
BackgroundMethodInfluentialKooiker, C. L., Birnie, M. T., & Baram, T. Z. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.673162 · Cited by 29 · see citing works
Hartmann, M. C., & Pleil, K. E. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108748 · Cited by 29 · see citing works
Li, S., Dong, X., & Kirouac, G. J. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02289-6 · Cited by 28 · see citing works
“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).”
BackgroundMethodResultInfluentialSelf-citationYe, Q., Nunez, J., & Zhang, X. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2042-21.2022 · Cited by 28 · see citing works
Dong, X., Li, S., & Kirouac, G. J. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100266 · Cited by 26 · see citing works
“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).”
InfluentialSelf-citationOrsini, C. A., Brown, T. E., Hodges, T. E., Alonso‐Caraballo, Y., Winstanley, C. A., & Becker, J. B. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1378-22.2022 · Cited by 26 · see citing works
Carr, K. D. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112850 · Cited by 22 · see citing works
“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
Beas, B. S., Khan, I., Gao, C., Loewinger, G. C., Macdonald, E., Bashford, A., Rodriguez-Gonzalez, S., Pereira, F., & Penzo, M. A. (2024) · Current Biology · doi:10.1016/j.cub.2024.02.037 · Cited by 24 · see citing works
Harris, N. A., & Winder, D. G. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00169 · Cited by 22 · see citing works
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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.”
BackgroundMethodViena, T. D., Rasch, G. E., & Allen, T. A. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02478-x · Cited by 22 · see citing works
“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
Perez, S. M., & Lodge, D. J. (2020) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa080 · Cited by 20 · see citing works
“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 19 · see citing works
“These subnuclei have diverse functions physiologically and have been shown in disease models of BD to react differentially to pathological mechanisms (30, 31).”
BackgroundGargiulo, A. T., Pirino, B. E., Curtis, G. R., & Barson, J. R. (2020) · Addiction Biology · doi:10.1111/adb.12972 · Cited by 21 · see citing works
“injected bilaterally in the NAc shell with the PACAP receptor antagonists, PACAP (6-27) and PACAP (6-38) (20 and 200 ρmol/side).”
BackgroundMethodInfluentialChoi, E. A., Husić, M., Millan, E. Z., Gilchrist, S., Power, J., Jean-Richard-dit-Bressel, P., & McNally, G. P. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0088-22.2022 · Cited by 20 · see citing works
Kooiker, C. L., Chen, Y., Birnie, M. T., & Baram, T. Z. (2023) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2023.01.002 · Cited by 20 · see citing works
“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
McDevitt, D. S., & Graziane, N. (2019) · eNeuro · doi:10.1523/eneuro.0377-19.2019 · Cited by 20 · see citing works
“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).”
BackgroundWang, T., Yan, R., Zhang, X., Wang, Z., Duan, H., Wang, Z., & Zhou, Q. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1028-22.2023 · Cited by 19 · see citing works
Deng, J. F., Chen, L., Liu, C., Liu, M., Guo, G., Wei, J., Zhang, J., Fan, H.-T., Zheng, Z., Yan, P., et al. (2024) · Advanced Science · doi:10.1002/advs.202401855 · Cited by 18 · see citing works
Cui, J.-J., Wang, J., Xu, D.-S., Xu, D., Guo, Y.-T., Guo, Y., Su, Y., Wang, Y.-Q., Jing, X.-H., & Bai, W.-Z. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.337055 · Cited by 17 · see citing works
“…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 18 · see citing works
“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 · see citing works
“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 · see citing works
Li, S. H., Li, S., & Kirouac, G. J. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.11.033 · Cited by 15 · see citing works
“…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 · see citing works
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 · see citing works
“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 14 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
Kirouac, G. J., Li, S., & Li, S. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02534-6 · Cited by 11 · see citing works
“…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 · see citing works
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Petersen, D., Raudales, R., Silva, A. K., Kellendonk, C., & Canetta, S. (2024) · eNeuro · doi:10.1523/eneuro.0284-24.2024 · Cited by 8 · see citing works
“…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 · see citing works
Rat Paraventricular Neurons Encode Predictive and Incentive Information of Reward Cues
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Hill-Bowen, L. D., Flannery, J. S., & Poudel, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1945-19.2019 · Cited by 8 · see citing works
“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 8 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
Activation patterns in male and female forebrain circuitries during food consumption under novelty
Greiner, E. M., Witt, M. E., Moran, S. J., & Petrovich, G. D. (2024) · Brain Structure and Function · doi:10.1007/s00429-023-02742-8 · Cited by 7 · see citing works
“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
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“…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 · see citing works
“…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) · doi:10.31219/osf.io/8cmhg · Cited by 5 · see citing works
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 · see citing works
- 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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