Skip to main content
Top
Published in: Brain Structure and Function 9/2017

01-12-2017 | Original Article

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

Authors: Xinwen Dong, Sa Li, Gilbert J. Kirouac

Published in: Brain Structure and Function | Issue 9/2017

Login to get access

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.
Literature
go back to reference Barson JR, Ho HT, Leibowitz SF (2015) Anterior thalamic paraventricular nucleus is involved in intermittent access ethanol drinking: role of orexin receptor 2. Addict Biol 20:469–481. doi:10.1111/adb.12139 CrossRefPubMed Barson JR, Ho HT, Leibowitz SF (2015) Anterior thalamic paraventricular nucleus is involved in intermittent access ethanol drinking: role of orexin receptor 2. Addict Biol 20:469–481. doi:10.​1111/​adb.​12139 CrossRefPubMed
go back to reference Barson JR, Poon K, Ho HT, Alam MI, Sanzalone L, Leibowitz SF (2017) Substance P in the anterior thalamic paraventricular nucleus: promotion of ethanol drinking in response to orexin from the hypothalamus. Addict Biol 22:58–69. doi:10.1111/adb.12288 CrossRefPubMed Barson JR, Poon K, Ho HT, Alam MI, Sanzalone L, Leibowitz SF (2017) Substance P in the anterior thalamic paraventricular nucleus: promotion of ethanol drinking in response to orexin from the hypothalamus. Addict Biol 22:58–69. doi:10.​1111/​adb.​12288 CrossRefPubMed
go back to reference Bentivoglio M, Balercia G, Kruger L (1991) The specificity of the nonspecific thalamus: the midline nuclei. Prog Brain Res 87:53–80CrossRefPubMed Bentivoglio M, Balercia G, Kruger L (1991) The specificity of the nonspecific thalamus: the midline nuclei. Prog Brain Res 87:53–80CrossRefPubMed
go back to reference Berendse HW, Groenewegen HJ (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299:187–228CrossRefPubMed Berendse HW, Groenewegen HJ (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299:187–228CrossRefPubMed
go back to reference Bubser M, Deutch AY (1998) Thalamic paraventricular nucleus neurons collateralize to innervate the prefrontal cortex and nucleus accumbens. Brain Res 787:304–310CrossRefPubMed Bubser M, Deutch AY (1998) Thalamic paraventricular nucleus neurons collateralize to innervate the prefrontal cortex and nucleus accumbens. Brain Res 787:304–310CrossRefPubMed
go back to reference Chen S, Aston-Jones G (1995) Evidence that cholera toxin B subunit (CTb) can be avidly taken up and transported by fibers of passage. Brain Res 674:107–111CrossRefPubMed Chen S, Aston-Jones G (1995) Evidence that cholera toxin B subunit (CTb) can be avidly taken up and transported by fibers of passage. Brain Res 674:107–111CrossRefPubMed
go back to reference Conte WL, Kamishina H, Reep RL (2009) The efficacy of the fluorescent conjugates of cholera toxin subunit B for multiple retrograde tract tracing in the central nervous system. Brain Struct Funct 213:367–373. doi:10.1007/s00429-009-0212-x CrossRefPubMed Conte WL, Kamishina H, Reep RL (2009) The efficacy of the fluorescent conjugates of cholera toxin subunit B for multiple retrograde tract tracing in the central nervous system. Brain Struct Funct 213:367–373. doi:10.​1007/​s00429-009-0212-x CrossRefPubMed
go back to reference Do-Monte FH, Minier-Toribio AM, Quiñones-Laracuente K, Medina-Colón EM, Quirk GJ (2017) Thalamic regulation of sucrose seeking during unexpected reward omission. Neuron 94:388–400.e4. doi:10.1016/j.neuron.2017.03.036 Do-Monte FH, Minier-Toribio AM, Quiñones-Laracuente K, Medina-Colón EM, Quirk GJ (2017) Thalamic regulation of sucrose seeking during unexpected reward omission. Neuron 94:388–400.e4. doi:10.​1016/​j.​neuron.​2017.​03.​036
go back to reference Groenewegen HJ, Berendse HW (1994) The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci 17:52–57CrossRefPubMed Groenewegen HJ, Berendse HW (1994) The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci 17:52–57CrossRefPubMed
go back to reference Hamlin AS, Clemens KJ, Choi EA, McNally GP (2009) Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur J Neurosci 29:802–812CrossRefPubMed Hamlin AS, Clemens KJ, Choi EA, McNally GP (2009) Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur J Neurosci 29:802–812CrossRefPubMed
go back to reference Heydendael W, Sharma K, Iyer V, Luz S, Piel D, Beck S, Bhatnagar S (2011) Orexins/hypocretins act in the posterior paraventricular thalamic nucleus during repeated stress to regulate facilitation to novel stress. Endocrinology 152:4738–4752. doi:10.1210/en.2011-1652 CrossRefPubMedPubMedCentral Heydendael W, Sharma K, Iyer V, Luz S, Piel D, Beck S, Bhatnagar S (2011) Orexins/hypocretins act in the posterior paraventricular thalamic nucleus during repeated stress to regulate facilitation to novel stress. Endocrinology 152:4738–4752. doi:10.​1210/​en.​2011-1652 CrossRefPubMedPubMedCentral
go back to reference Hsu DT, Price JL (2009) Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 512:825–848CrossRefPubMedPubMedCentral Hsu DT, Price JL (2009) Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 512:825–848CrossRefPubMedPubMedCentral
go back to reference Li S, Kirouac GJ (2008) Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 506:263–287CrossRefPubMed Li S, Kirouac GJ (2008) Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 506:263–287CrossRefPubMed
go back to reference Li Y, Li S, Sui N, Kirouac GJ (2009) Orexin-A acts on the paraventricular nucleus of the midline thalamus to inhibit locomotor activity in rats. Pharmacol Biochem Behav 93:506–514CrossRefPubMed Li Y, Li S, Sui N, Kirouac GJ (2009) Orexin-A acts on the paraventricular nucleus of the midline thalamus to inhibit locomotor activity in rats. Pharmacol Biochem Behav 93:506–514CrossRefPubMed
go back to reference Li Y, Li S, Wei C, Wang H, Sui N, Kirouac GJ (2010a) Changes in emotional behavior produced by orexin microinjections in the paraventricular nucleus of the thalamus. Pharmacol Biochem Behav 95:121–128CrossRefPubMed Li Y, Li S, Wei C, Wang H, Sui N, Kirouac GJ (2010a) Changes in emotional behavior produced by orexin microinjections in the paraventricular nucleus of the thalamus. Pharmacol Biochem Behav 95:121–128CrossRefPubMed
go back to reference Luppi PH, Fort P, Jouvet M (1990) Iontophoretic application of unconjugated cholera toxin B subunit (CTb) combined with immunohistochemistry of neurochemical substances: a method for transmitter identification of retrogradely labeled neurons. Brain Res 534:209–224CrossRefPubMed Luppi PH, Fort P, Jouvet M (1990) Iontophoretic application of unconjugated cholera toxin B subunit (CTb) combined with immunohistochemistry of neurochemical substances: a method for transmitter identification of retrogradely labeled neurons. Brain Res 534:209–224CrossRefPubMed
go back to reference Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221–238CrossRefPubMed Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221–238CrossRefPubMed
go back to reference Nicola SM (2007) The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology 191:521–550CrossRefPubMed Nicola SM (2007) The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology 191:521–550CrossRefPubMed
go back to reference Otake K, Nakamura Y (1998) Single midline thalamic neurons projecting to both the ventral striatum and the prefrontal cortex in the rat. Neuroscience 86:635–649CrossRefPubMed Otake K, Nakamura Y (1998) Single midline thalamic neurons projecting to both the ventral striatum and the prefrontal cortex in the rat. Neuroscience 86:635–649CrossRefPubMed
go back to reference Parent A, Sato F, Wu Y, Gauthier J, Levesque M, Parent M (2000) Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci 23:S20–S27CrossRefPubMed Parent A, Sato F, Wu Y, Gauthier J, Levesque M, Parent M (2000) Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci 23:S20–S27CrossRefPubMed
go back to reference Paxinos G, Watson C (2009) The rat brain in stereotaxic coordinates, 6th edn. Elsevier Academic Press, San Diego Paxinos G, Watson C (2009) The rat brain in stereotaxic coordinates, 6th edn. Elsevier Academic Press, San Diego
go back to reference Pennartz CM, Groenewegen HJ, Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719–761CrossRefPubMed Pennartz CM, Groenewegen HJ, Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719–761CrossRefPubMed
go back to reference Prensa L, Gimenez-Amaya JM, Parent A, Bernacer J, Cebrian C (2009) The nigrostriatal pathway: axonal collateralization and compartmental specificity. J Neural Transm Suppl:49–58 Prensa L, Gimenez-Amaya JM, Parent A, Bernacer J, Cebrian C (2009) The nigrostriatal pathway: axonal collateralization and compartmental specificity. J Neural Transm Suppl:49–58
go back to reference Reichard RA et al (2016) Abundant collateralization of temporal lobe projections to the accumbens, bed nucleus of stria terminalis, central amygdala and lateral septum. Brain Struct Funct. doi:10.1007/s00429-016-1321-y PubMed Reichard RA et al (2016) Abundant collateralization of temporal lobe projections to the accumbens, bed nucleus of stria terminalis, central amygdala and lateral septum. Brain Struct Funct. doi:10.​1007/​s00429-016-1321-y PubMed
go back to reference Reynolds SM, Berridge KC (2008) Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci 11:423–425CrossRefPubMedPubMedCentral Reynolds SM, Berridge KC (2008) Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci 11:423–425CrossRefPubMedPubMedCentral
go back to reference Shinonaga Y, Takada M, Mizuno N (1994) Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat. Neuroscience 58:389–397CrossRefPubMed Shinonaga Y, Takada M, Mizuno N (1994) Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat. Neuroscience 58:389–397CrossRefPubMed
go back to reference Smith Y, Raju DV, Pare JF, Sidibe M (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 27:520–527CrossRefPubMed Smith Y, Raju DV, Pare JF, Sidibe M (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 27:520–527CrossRefPubMed
go back to reference Su HS, Bentivoglio M (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J Comp Neurol 297:582–593CrossRefPubMed Su HS, Bentivoglio M (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J Comp Neurol 297:582–593CrossRefPubMed
go back to reference Unzai T, Kuramoto E, Kaneko T, Fujiyama F (2017) Quantitative analyses of the projection of individual neurons from the midline thalamic nuclei to the striosome and matrix compartments of the rat striatum. Cereb Cortex 27:1164–1181. doi:10.1093/cercor/bhv295 Unzai T, Kuramoto E, Kaneko T, Fujiyama F (2017) Quantitative analyses of the projection of individual neurons from the midline thalamic nuclei to the striosome and matrix compartments of the rat striatum. Cereb Cortex 27:1164–1181. doi:10.​1093/​cercor/​bhv295
go back to reference Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39:107–140CrossRefPubMed Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39:107–140CrossRefPubMed
go back to reference Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212–237CrossRefPubMed Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212–237CrossRefPubMed
go back to reference Young CD, Deutch AY (1998) The effects of thalamic paraventricular nucleus lesions on cocaine-induced locomotor activity and sensitization. Pharmacol Biochem Behav 60:753–758CrossRefPubMed Young CD, Deutch AY (1998) The effects of thalamic paraventricular nucleus lesions on cocaine-induced locomotor activity and sensitization. Pharmacol Biochem Behav 60:753–758CrossRefPubMed
Metadata
Title
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
Authors
Xinwen Dong
Sa Li
Gilbert J. Kirouac
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 9/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1445-8

Other articles of this Issue 9/2017

Brain Structure and Function 9/2017 Go to the issue