Brainstem projections to midline and intralaminar thalamic nuclei of the rat
Abstract
The projections from the brainstem to the midline and intralaminar thalamic nuclei were examined in the rat. Stereotaxic injections of the retrograde tracer cholera toxin beta -subunit (CTb) were made in each of the intralaminar nuclei of the dorsal thalamus: the lateral parafascicular, medial parafascicular, central lateral, paracentral, oval paracentral, and central medial nuclei; in the midline thalamic nuclei-the paraventricular, intermediodorsal, mediodorsal, paratenial, rhomboid, reuniens, and submedius nuclei; and, in the anteroventral, parvicellular part of the ventral posterior, and caudal ventral medial nuclei. The retrograde cell body labeling pattern within the brainstem nuclei was then analyzed. Nearly every thalamic site received a projection from the deep mesencephalic reticular, pedunculopontine tegmental, dorsal raphe, median raphe, laterodorsal tegmental, and locus coeruleus nuclei. Most intralaminar thalamic sites were also innervated by unique combinations of medullary and pontine reticular formation nuclei such as the subnucleus reticularis dorsalis, gigantocellular, dorsal paragigantocellular, lateral, parvicellular, caudal pontine, ventral pontine, and oral pontine reticular nuclei; the dorsomedial tegmental, subpeduncular tegmental, and ventral tegmental areas; and, the central tegmental field. In addition, most intralaminar injections resulted in retrograde cell body labeling in the substantia nigra, nucleus Darkschewitsch, interstitial nucleus of Cajal, and cuneiform nucleus. Details concerning the pathways from the spinal trigeminal, nucleus tractus solitarius, raphe magnus, raphe pallidus, and the rostral and caudal linear raphe nuclei to subsets of midline and intralaminar thalamic sites are discussed in the text. The discussion focuses on brainstem-thalamic pathways that are likely involved in arousal, somatosensory, and visceral functions.
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The reticular arousal systems control alertness and orientation in different contexts and interface strongly with the limbic system, autonomic nervous system, and emotional motor system.
“It controls alertness and orientation in different contexts, and interfaces strongly with LS, ANS and EMS (Krout et al., 2002; Berntson and Cacioppo, 2007).”
From Somatic experiencing: using interoception and proprioception as core elements of trauma therapy (2015) · cites this paper as Krout et al., 2002
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Hypothalamic regulation of sleep and circadian rhythms
Saper, C. B., Scammell, T. E., & Lu, J. (2005) · Nature · doi:10.1038/nature04284 · Cited by 2,804 · see citing works
Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat
Hoover, W. B., & Vertes, R. P. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0150-4 · Cited by 1,365 · see citing works
General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal
Franks, N. P. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2372 · Cited by 1,266 · see citing works
Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease
Redgrave, P., Rodriguez, M., Smith, Y., Rodriguez-Oroz, M. C., Lehericy, S., Bergman, H., Agid, Y., DeLong, M. R., & Obeso, J. A. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2915 · Cited by 1,134 · see citing works
Heidbreder, C. A., & Groenewegen, H. J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.09.003 · Cited by 882 · see citing works
The short-latency dopamine signal: a role in discovering novel actions?
Redgrave, P., & Gurney, K. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2022 · Cited by 762 · see citing works
Unresponsiveness ≠ unconsciousness
Sanders, R. D., Tononi, G., Laureys, S., Sleigh, J. W., & Warner, D. S. (2012) · Anesthesiology · doi:10.1097/aln.0b013e318249d0a7 · Cited by 474 · see citing works
Schiff, N. D. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.029 · Cited by 463 · see citing works
Subcortical loops through the basal ganglia
McHaffie, J. G., Stanford, T. R., Stein, B. E., Coizet, V., & Redgrave, P. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.06.006 · Cited by 419 · see citing works
Limbic circuitry of the midline thalamus
Vertes, R. P., Linley, S. B., & Hoover, W. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.014 · Cited by 391 · see citing works
The paraventricular thalamus is a critical thalamic area for wakefulness
Ren, S., Wang, Y., Yue, F., Cheng, X., Dang, R., Qiao, Q., Sun, X., Li, X., Jiang, Q., Yao, J., et al. (2018) · Science · doi:10.1126/science.aat2512 · Cited by 366 · see citing works
Placing the paraventricular nucleus of the thalamus within the brain circuits that control behavior
Kirouac, G. J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.08.005 · Cited by 357 · see citing works
Vertes, R. P., Hoover, W. B., Szigeti‐Buck, K., & Léránth, C. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.12.002 · Cited by 345 · see citing works
Somatic experiencing: using interoception and proprioception as core elements of trauma therapy
Payne, P., Levine, P. A., & Crane-Godreau, M. A. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00093 · Cited by 344 · see citing works
Saper, C. B., & Stornetta, R. L. (2004) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00023-1 · Cited by 321 · see citing works
Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat
Vertes, R. P., Hoover, W. B., Valle, A. C., Sherman, A., & Rodriguez, J. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21135 · Cited by 305 · see citing works
Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat
Vertes, R. P., & Hoover, W. B. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21679 · Cited by 296 · see citing works
Neurophysiology of sleep and wakefulness: basic science and clinical implications
Schwartz, J., & Roth, T. (2008) · Current Neuropharmacology · doi:10.2174/157015908787386050 · Cited by 289 · see citing works
Li, S., & Kirouac, G. J. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21502 · Cited by 261 · see citing works
Afferent projections to nucleus reuniens of the thalamus
McKenna, J. T., & Vertes, R. P. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20342 · Cited by 272 · see citing works
Breathing as a fundamental rhythm of brain function.
Heck, D. H., McAfee, S. S., Liu, Y., Babajani-Feremi, A., Rezaie, R., Freeman, W. J., Wheless, J. W., Papanicolaou, A. C., Ruszinkó, M., Sokolov, Y., et al. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00115 · Cited by 272 · see citing works
Hale, M. W., & Lowry, C. A. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2089-z · Cited by 243 · see citing works
Thalamic dual control of sleep and wakefulness
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Topographical Organization of the Pedunculopontine Nucleus
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Brain circuits for pain and its treatment
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Li, S., & Kirouac, G. J. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0360-7 · Cited by 230 · see citing works
Noradrenergic Locus Coeruleus pathways in pain modulation
Llorca-Torralba, M., Borges, G., Neto, F. L. M., Micó, J. A., & Berrocoso, E. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.057 · Cited by 230 · see citing works
Basal ganglia circuit loops, dopamine and motivation: a review and enquiry
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Randomized controlled trial of trigeminal nerve stimulation for drug-resistant epilepsy
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The pontine REM switch: past and present
Fuller, P. M., Saper, C. B., & Lu, J. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.140160 · Cited by 211 · see citing works
Hale, M. W., Shekhar, A., & Lowry, C. A. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9827-1 · Cited by 210 · see citing works
Cassel, J., de Vasconcelos, A. P., Loureiro, M., Cholvin, T., Dalrymple‐Alford, J. C., & Vertes, R. P. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.08.006 · Cited by 202 · see citing works
A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement
Inagaki, H., Chen, S., Ridder, M. C., Sah, P., Li, N., Yang, Z., Hasanbegović, H., Gao, Z., Gerfen, C. R., & Svoboda, K. (2022) · Cell · doi:10.1016/j.cell.2022.02.006 · Cited by 207 · see citing works
Staying awake for dinner: hypothalamic integration of sleep, feeding, and circadian rhythms
Saper, C. B. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)53014-6 · Cited by 178 · see citing works
Hoover, W. B., & Vertes, R. P. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0345-6 · Cited by 178 · see citing works
McElvain, L. E., Chen, Y., Moore, J. D., Brigidi, G. S., Bloodgood, B. L., Lim, B. K., Costa, R. M., & Kleinfeld, D. (2021) · Neuron · doi:10.1016/j.neuron.2021.03.017 · Cited by 158 · see citing works
Waite, P. M. E., & Ashwell, K. W. S. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374236-0.10031-8 · Cited by 158 · see citing works
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Orexin (hypocretin) innervation of the paraventricular nucleus of the thalamus
Kirouac, G. J., Parsons, M. P., & Li, S. (2005) · Brain Research · doi:10.1016/j.brainres.2005.08.035 · Cited by 157 · see citing works
Conte, W. L., Kamishina, H., & Reep, R. L. (2009) · Nature Protocols · doi:10.1038/nprot.2009.93 · Cited by 153 · see citing works
Improved method for combination of immunocytochemistry and Nissl staining
Kádár, A., Wittmann, G., Liposits, Z., & Fekete, C. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.07.010 · Cited by 150 · see citing works
Cognitive enhancement with central thalamic electrical stimulation
Shirvalkar, P. R., Seth, M. I., Schiff, N. D., & Herrera, D. G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604811103 · Cited by 148 · see citing works
Basic Anatomy and Physiology of Pain Pathways
Bick, S. K. B., Machado, A. G., & Nagel, S. J. (2014) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2014.06.001 · Cited by 142 · see citing works
A Hypothalamic Switch for REM and Non-REM Sleep
Chen, K.-S., Xu, M., Zhang, Z., Chang, W.-C., Gaj, T., Schaffer, D. V., & Dan, Y. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.005 · Cited by 137 · see citing works
Parsons, M. P., Li, S., & Kirouac, G. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21224 · Cited by 141 · see citing works
Kirouac, G. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.627633 · Cited by 137 · see citing works
Hahn, J. D., & Swanson, L. W. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.02.002 · Cited by 121 · see citing works
Glucagon‐like peptide‐1 in the rat brain: Distribution of expression and functional implication
Gu, G., Roland, B. L., Tomaselli, K. J., Dolman, C. S., Lowe, C., & Heilig, J. S. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23282 · Cited by 119 · see citing works
Drivers of the Primate Thalamus
Rovó, Z., Ulbert, I., & Acsády, L. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2815-12.2012 · Cited by 116 · see citing works
Wolff, S. B. E., Ko, R., & Ölveczky, B. P. (2022) · Science Advances · doi:10.1126/sciadv.abk0231 · Cited by 115 · see citing works
Ballanger, B., Lozano, A. M., Moro, E., van Eimeren, T., Hamani, C., Chen, R. E., Cilia, R., Houle, S., Poon, Y. Y., Lang, A. E., et al. (2009) · Human Brain Mapping · doi:10.1002/hbm.20815 · Cited by 114 · see citing works
Colavito, V., Tesoriero, C., Wirtu, A. T., Grassi-Zucconi, G., & Bentivoglio, M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.021 · Cited by 117 · see citing works
Alkire, M. T., Asher, C. D., Franciscus, A. M., & Hahn, E. L. (2009) · Anesthesiology · doi:10.1097/aln.0b013e31819c461c · Cited by 105 · see citing works
Distribution of Dopamine D2-Like Receptors in the Human Thalamus: Autoradiographic and PET Studies
Rieck, R. W., Ansari, M. S., Whetsell, W. O., Deutch, A. Y., & KESSLER, R. M. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300336 · Cited by 100 · see citing works
Hsu, D. T., & Price, J. L. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21440 · Cited by 97 · see citing works
Ishibashi, M., Takano, S., Yanagida, H., Takatsuna, M., Nakajima, K., Oomura, Y., Wayner, M. J., & Sasaki, K. (2004) · Peptides · doi:10.1016/j.peptides.2004.10.014 · Cited by 96 · see citing works
Vegetative State and Minimally Conscious State: A Review of the Therapeutic Interventions
Georgiopoulos, M., Katsakiori, P. F., Kefalopoulou, Z. M., Ellul, J., Chroni, E., & Constantoyannis, C. (2010) · Stereotactic and Functional Neurosurgery · doi:10.1159/000314354 · Cited by 98 · see citing works
Medial vestibular connections with the hypocretin (orexin) system
Horowitz, S. S., Blanchard, J. H., & Morin, L. P. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20521 · Cited by 97 · see citing works
Chen, W.-K., Liu, I. Y., Chang, Y.-T., Chen, Y.-C., Chen, C., Yen, C., Shin, H., & Chen, C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1041-10.2010 · Cited by 96 · see citing works
Krout, K. E., Mettenleiter, T. C., & Loewy, A. D. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00997-1 · Cited by 96 · see citing works
Vertes, R. P., Hoover, W. B., & Rodriguez, J. J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.067 · Cited by 95 · see citing works
Corticotropin-releasing factor-related peptides, serotonergic systems, and emotional behavior
Fox, J. H., & Lowry, C. A. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00169 · Cited by 93 · see citing works
Parsons, M. P., Li, S., & Kirouac, G. J. (2006) · Synapse · doi:10.1002/syn.20264 · Cited by 93 · see citing works
Cicco, V. D., Fantozzi, M. P. T., Cataldo, E., Barresi, M., Bruschini, L., Faraguna, U., & Manzoni, D. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00130 · Cited by 91 · see citing works
Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win‐shift performance
Hembrook‐Short, J. R., & Mair, R. G. (2010) · Hippocampus · doi:10.1002/hipo.20797 · Cited by 89 · see citing works
Mátyás, F., Lee, J.-H., Shin, H., & Acsády, L. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12610 · Cited by 88 · see citing works
The pedunculopontine nucleus as a target for deep brain stimulation
Hamani, C., Moro, E., & Lozano, A. M. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0547-8 · Cited by 85 · see citing works
Messier, M. L., Li, A., & Nattie, E. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00805.2003 · Cited by 84 · see citing works
Jiménez-Sánchez, L., Castañé, A., Pérez-Caballero, L., Grifoll, M., López-Gil, X., Campa, L., Galofré, M., Berrocoso, E., & Adell, A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv133 · Cited by 83 · see citing works
Major diencephalic inputs to the hippocampus
Vertes, R. P. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.008 · Cited by 83 · see citing works
A subcortical inhibitory signal for behavioral arrest in the thalamus
Giber, K., Diana, M. A., Plattner, V. M., Dugué, G. P., Bokor, H., Rousseau, C. V., Maglóczky, Z., Havas, L., Hangya, B., Wildner, H., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3951 · Cited by 83 · see citing works
Structural and functional organization of the midline and intralaminar nuclei of the thalamus
Vertes, R. P., Linley, S. B., & Rojas, A. K. P. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.964644 · Cited by 82 · see citing works
Central mechanisms of cranial nerve stimulation for epilepsy
Fanselow, E. E. (2012) · Surgical Neurology International · doi:10.4103/2152-7806.103014 · Cited by 80 · see citing works
Hembrook‐Short, J. R., Onos, K. D., & Mair, R. G. (2011) · Hippocampus · doi:10.1002/hipo.20945 · Cited by 80 · see citing works
Sukhotinsky, I., Zalkind, V. I., Lu, J., Hopkins, D. A., Saper, C. B., & Devor, M. G. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05399.x · Cited by 80 · see citing works
Distribution of norepinephrine transporters in the non-human primate brain
Smith, H. R., Beveridge, T. J. R., & Porrino, L. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.11.033 · Cited by 79 · see citing works
Raison, C. L., Hale, M. W., Williams, L. E., Wager, T. D., & Lowry, C. A. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01580 · Cited by 76 · see citing works
Prefrontal modulation of anxiety through a lens of noradrenergic signaling
Bouras, N. N., Mack, N. R., & Gao, W. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1173326 · Cited by 81 · see citing works
Integrating brainstem and cortical functional architectures
Hansen, J. Y., Cauzzo, S., Singh, K., García‐Gomar, M. G., Shine, J. M., Bianciardi, M., & Mišić, B. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01787-0 · Cited by 83 · see citing works
Matzeu, A., Zamora-Martinez, E. R., & Martin‐Fardon, R. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00117 · Cited by 81 · see citing works
Leite‐Almeida, H., Valle‐Fernandes, A., & Almeida, A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.022 · Cited by 75 · see citing works
Lowry, C. A., Evans, A. K., Gasser, P. J., Hale, M. W., Staub, D. R., & Shekhar, A. (2008) · Birkhäuser Basel eBooks · doi:10.1007/978-3-7643-8561-3_2 · Cited by 75 · see citing works
Human cardiovascular and gustatory brainstem sites observed by functional magnetic resonance imaging
Topolovec‐Vranic, J., Gati, J. S., Menon, R. S., Shoemaker, J. K., & Cechetto, D. F. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20033 · Cited by 74 · see citing works
Bailey, K. R., & Mair, R. G. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.2.410 · Cited by 74 · see citing works
Jang, S. H., Lim, H. W., & Yeo, S. S. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.07.024 · Cited by 73 · see citing works
The midline and intralaminar thalamic nuclei
Benarroch, E. E. (2008) · Neurology · doi:10.1212/01.wnl.0000326066.57313.13 · Cited by 74 · see citing works
Short-Latency Activation of Striatal Spiny Neurons via Subcortical Visual Pathways
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The nonspecific thalamus: A place in a wedding bed for making memories last?
de Vasconcelos, A. P., & Cassel, J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.021 · Cited by 68 · see citing works
Pattern of distribution of serotonergic fibers to the thalamus of the rat
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Molecular anatomy of the thalamic complex and the underlying transcription factors
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Small animal, whole brain fMRI: Innocuous and nociceptive forepaw stimulation
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The pedunculopontine nucleus and movement disorders: Anatomy and the role for deep brain stimulation
Hamani, C., Stone, S. S. D., Laxton, A. W., & Lozano, A. M. (2007) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(08)70016-6 · Cited by 65 · see citing works
Efferent and afferent connections of the dorsal and median raphe nuclei in the rat
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Yasukawa, T., Kita, T., Xue, Y., & Kita, H. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20029 · Cited by 62 · see citing works
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- Authors
- Krout, K. E., Belzer, R. E., & Loewy, A. D.
- Affiliations
- Washington University in St. Louis (US)
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2002-05-07
- Volume
- 448
- Issue
- 1
- Pages
- 53-101
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1997269000
- Cited by
- 328
- References
- 116
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 12 · 2023: 15 · 2022: 6 · 2021: 22 · 2020: 17 · 2019: 16 · 2018: 13 · 2017: 13 · 2016: 7 · 2015: 20 · 2014: 11 · 2013: 10 · 2012: 11
- FWCI
- 4.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL25449)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- midline thalamic nuclei, intralaminar nuclei, dorsal thalamus, retrograde tracing, reticular formation, pedunculopontine nucleus, locus coeruleus, substantia nigra, interstitial nucleus of Cajal, cuneiform nucleus, raphe nuclei, arousal, somatosensory pathways, rats
- MeSH terms
- Animals, Arousal, Attention, Autonomic Nervous System, Brain Mapping, Brain Stem, Cerebral Cortex, Cholera Toxin, Male, Neural Pathways, Neurons, Pain, Raphe Nuclei, Reticular Formation, Sleep, Tegmentum Mesencephali, Rats, Sprague-Dawley, Midline Thalamic Nuclei, Intralaminar Thalamic Nuclei, Rats
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