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Chapter 3 - Thalamic Output Pathways

from Section 2: - Anatomy

Published online by Cambridge University Press:  12 August 2022

Michael M. Halassa
Affiliation:
Massachusetts Institute of Technology
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Summary

Projection neurons are both the main target of inputs to the thalamus and the only conduit for thalamic outputs. Projection neurons show similar somatodendritic morphologies, electrotonic properties, and membrane conductances, and they are all glutamatergic. Moreover, their axons never cross the midline and always target both the prethalamic reticular nucleus and one or more forebrain structures, chiefly the cerebral cortex and/or striatum. Despite these similarities, however, new anatomical, electrophysiological, and transcriptomic methods with single-cell resolution have in recent years revealed that thalamic projection neurons are remarkably diverse. Differences prominently involve axon arborization and gene-expression patterns, but significant variations in somatodendritic morphology and membrane conductances are also evident. Here, I first review the structural, functional, and gene-expression single-cell level variation observed among thalamic projection neurons. Then, based on evidence currently available for rodents, I propose a tentative catalog of six high-level cell classes. This catalog provides a consistent and cellularly accurate framework for the analysis of classic, large-scale thalamic output pathways such as the thalamocortical, thalamostriatal, and thalamoamygdaloid, among others. Moreover, developmental studies suggest that the neuron classes identified here may reflect a fundamental level of cell-lineage diversity that precedes nuclei formation or the establishment of thalamus connection systems.

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The Thalamus , pp. 45 - 70
Publisher: Cambridge University Press
Print publication year: 2022

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References

Adams, NC, Lozsádi, DA, Guillery, RW. (1997) Complexities in the thalamocortical and corticothalamic pathways. Eur J Neurosci. 9:204209.Google Scholar
Aguilar, J, Morales-Botello, ML, Foffani, G. (2008) Tactile responses of hindpaw, forepaw and whisker neurons in the thalamic ventrobasal complex of anesthetized rats. Eur J Neurosci. 27:378387.Google Scholar
Arbuthnott, GW, MacLeod, NK, Maxwell, DJ, Wright, AK. (1990) Distribution and synaptic contacts of the cortical terminals arising from neurons in the rat ventromedial thalamic nucleus. Neuroscience. 38:4760.Google Scholar
Asanuma, C, Andersen, RA, Cowan, WM. (1985) The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: divergent cortical projections from cell clusters in the medial pulvinar nucleus. J Comp Neurol. 241:357381. doi: 10.1002/cne.902410309.CrossRefGoogle ScholarPubMed
Avendaño, C, Stepniewska, I, Rausell, E, Reinoso-Suárez, F. (1990) Segregation and heterogeneity of thalamic cell populations projecting to superficial layers of posterior parietal cortex: a retrograde tracer study in cat and monkey. Neuroscience 39:547559.Google Scholar
Baimbridge, KG, Celio, MR, Rogers, JH. (1992) Calcium-binding proteins in the nervous system. Trends Neurosci. 15:303308. doi: 10.1016/0166-2236(92)90081-i.Google Scholar
Barroso-Chinea, P, Castle, M, Aymerich, MS, Pérez-Manso, M, Erro, E, Tuñon, T, Lanciego, JL. (2007) Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. J Comp Neurol. 501:703715. doi: 10.1002/cne.21265.Google Scholar
Bartlett, EL, Smith, PH. (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol. 81:19992016. doi: 10.1152/jn.1999.81.5.1999.Google Scholar
Bartlett, EL, Smith, PH. (2002) Effects of paired-pulse and repetitive stimulation on neurons in the rat medial geniculate body. Neuroscience. 113:957974. doi: 10.1016/s0306-4522(02)00240-3.Google Scholar
Beatty, JA, Sylwestrak, EL, Cox, CL. (2009) Two distinct populations of projection neurons in the rat lateral parafascicular thalamic nucleus and their cholinergic responsiveness. Neuroscience. 162:155173. doi: 10.1016/j.neuroscience.2009.04.043.CrossRefGoogle ScholarPubMed
Bonnefond, M, Kastner, S, Jensen, O. (2017) Communication between brain areas based on nested oscillations. eNeuro. Mar 27;4(2):ENEURO.0153–16.2017. doi: 10.1523/ENEURO.0153-16.2017.Google Scholar
Boyd, JD, Matsubara, JA. (1996) Laminar and columnar patterns of geniculocortical projections in the cat: relationship to cytochrome oxidase. J Comp Neurol. 365:659682.Google Scholar
Carey, RG, Fitzpatrick, D, Diamond, IT. (1979a) Thalamic projections to layer I of striate cortex shown by retrograde transport of horseradish peroxidase. Science. 203:556559.Google Scholar
Carey, RG, Fitzpatrick, D, Diamond, IT. (1979b) Layer I of striate cortex of Tupaia glis and Galago senegalensis: projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase. J Comp Neurol. 186:393437.Google Scholar
Carey, RG, Neal, TL. (1986) Reciprocal connections between the claustrum and visual thalamus in the tree shrew (Tupaia glis). Brain Res. 386:155168.Google Scholar
Casas-Torremocha, D, Porrero, C, Rodriguez-Moreno, J, García-Amado, M, Lübke, JHR, Núñez, Á, Clascá, F. (2019) Posterior thalamic nucleus axon terminals have different structure and functional impact in the motor and somatosensory vibrissal cortices. Brain Struct Funct. 224:16271645.Google Scholar
Castro-Alamancos, MA, Connors, BW. (1997) Thalamocortical synapses. Prog Neurobiol. 51(6):581606. doi: 10.1016/s0301-0082(97)00002-6.Google Scholar
Catalano, SM, Robertson, RT, Killackey, HP. (1996) Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J Comp Neurol. 367:3653. doi: 10.1002/(SICI)1096-9861(19960325)367:1<36::AID-CNE4>3.0.CO;2-K.Google Scholar
Clascá, F, Porrero, C, Galazo, M, Rubio-Garrido, P, Evangelio, M. (2016) Anatomy and development of multi-specific thalamocortical axons: implications for cortical dynamics and evolution. In Rockland, KS (ed.), Axons and Brain Architecture. Amsterdam: Elsevier, pp. 6992. doi: 10.1016/B978-0-12-801393-9.00004-9.Google Scholar
Clascá, F, Rubio-Garrido, P, Jabaudon, D. (2012). Unveiling the diversity of thalamocortical neuron subtypes. Eur J Neurosci. 35:15241532.Google Scholar
Clerici, WJ, McDonald, AJ, Thompson, R, Coleman, JR. (1990) Anatomy of the rat medial geniculate body: II. Dendritic morphology. J Comp Neurol. 297:3254.Google Scholar
Cruikshank, SJ, Ahmed, OJ, Stevens, TR, Patrick, SL, Gonzalez, AN, Elmaleh, M, Connors, BW. (2012) Thalamic control of layer 1 circuits in prefrontal cortex. J Neurosci. 32:1781317823. doi: 10.1523/JNEUROSCI.3231-12.2012.Google Scholar
Crunelli, V, Leresche, N, Parnavelas, JG. (1987) Membrane properties of morphologically identified X and Y cells in the lateral geniculate nucleus of the cat in vitro. J Physiol. 390:243256. doi: 10.1113/jphysiol.1987.sp016697.CrossRefGoogle ScholarPubMed
Crunelli, V, Lorincz, ML, Connelly, WM, David, F, Hughes, SW, Lambert, RC, Leresche, N, Errington, AC. (2018) Dual function of thalamic low-vigilance state oscillations: Rhythm-regulation and plasticity. Nat Rev Neurosci. 19:107118. doi: 10.1038/nrn.2017.151Google Scholar
Desai, NV, Varela, C. (2021) Distinct burst properties contribute to the functional diversity of thalamic nuclei. J Comp Neurol. 529(17): 37263750.Google Scholar
Deschênes, M, Bourassa, J, Doan, VD, Parent, A. (1996) A single-cell study of the axonal projections arising from the posterior intralaminar thalamic nuclei in the rat. Eur J Neurosci. 8:329343.Google Scholar
Deschênes, M, Bourassa, J, Parent, A. (1995) Two different types of thalamic fibers innervate the rat striatum. Brain Res. 701:288292.Google Scholar
Deschênes, M, Bourassa, J, Parent, A. (1996) Striatal and cortical projections of single neurons from the central lateral thalamic nucleus in the rat. Neuroscience. 72:679687.Google Scholar
Deschênes, M, Veinante, P, Zhang, ZW. (1998) The organization of corticothalamic projections: reciprocity versus parity. Brain Res Brain Res Rev. 28:286308. doi: 10.1016/s0165-0173(98)00017-4.Google Scholar
Donoghue, JP, Ebner, FF. (1981) The laminar distribution and ultrastructure of fibers projecting from three thalamic nuclei to the somatic sensory-motor cortex of the opossum. J Comp Neurol. 198:389420. doi: 10.1002/cne.901980303.Google Scholar
Doron, NN, Ledoux, JE. (2000) Cells in the posterior thalamus project to both amygdala and temporal cortex: a quantitative retrograde double-labeling study in the rat. J Comp Neurol. 425:257274.Google Scholar
Ellender, TJ, Harwood, J, Kosillo, P, Capogna, M, Bolam, JP. (2013) Heterogeneous properties of central lateral and parafascicular thalamic synapses in the striatum. J Physiol. 591:257272. doi: 10.1113/jphysiol.2012.245233.Google Scholar
Erro, M, Lanciego, JL, Gimenez-Amaya, JM. (2002) Re-examination of the thalamostriatal projections in the rat with retrograde tracers. Neurosci Res. 42:4555. doi: 10.1016/s0168-0102(01)00302-9.Google Scholar
Familtsev, D, Quiggins, R, Masterson, SP, Dang, W, Slusarczyk, AS, Petry, HM, Bickford, ME. (2016) Ultrastructure of geniculocortical synaptic connections in the tree shrew striate cortex. J Comp Neurol. 524:12921306. doi: 10.1002/cne.23907.Google Scholar
Ferster, D, LeVay, S. (1978) The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat. J Comp Neurol. 182:923944. doi: 10.1002/cne.901820510.Google Scholar
Fiebelkorn, IC, Pinsk, MA, Kastner, S. (2019) The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention. Nat Commun. 10:215. doi: 10.1038/s41467-018-08151-4.Google Scholar
Fitzpatrick, D, Itoh, K, Diamond, IT. (1983) The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). J Neurosci. 3:673702.CrossRefGoogle ScholarPubMed
Friedlander, MJ, Lin, CS, Stanford, LR, Sherman, SM. (1981) Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. J Neurophysiol. 46:80129. doi: 10.1152/jn.1981.46.1.80.Google Scholar
Fujiyama, F, Furuta, T, Kaneko, T. (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol. 435:379387. doi: 10.1002/cne.1037.Google Scholar
Furuta, T, Tomioka, R, Taki, K, Nakamura, K, Tamamaki, N, Kaneko, T. (2001) In vivo transduction of central neurons using recombinant Sindbis virus: Golgi-like labeling of dendrites and axons with membrane-targeted fluorescent proteins. J Histochem Cytochem. 49:14971508. doi: 10.1177/002215540104901203.Google Scholar
Galazo, MJ, Martinez-Cerdeño, V, Porrero, C, Clascá, F. (2008) Embryonic and postnatal development of the layer I-directed (“matrix”) thalamocortical system in the rat. Cereb Cortex. 18:344363.Google Scholar
Garel, S, López-Bendito, G. (2014) Inputs from the thalamocortical system on axon pathfinding mechanisms. Curr Opin Neurobiol. 27:143150. doi: 10.1016/j.conb.2014.03.013.Google Scholar
Garraghty, PE, Sur, M. (1990) Morphology of single intracellularly stained axons terminating in area 3b of macaque monkeys. J Comp Neurol. 294:583593. doi: 10.1002/cne.902940406. PMID: 2341626.CrossRefGoogle ScholarPubMed
Gheorghita, F, Kraftsik, R, Dubois, R, Welker, E. (2006) Structural basis for map formation in the thalamocortical pathway of the barrelless mouse. J Neurosci. 26:1005710067. doi: 10.1523/JNEUROSCI.1263-06.2006.Google Scholar
Graybiel, AM, Berson, DM. (1980) Histochemical identification and afferent connections of subdivisions in the lateralis posterior-pulvinar complex and related thalamic nuclei in the cat. Neuroscience. 5:11751238. doi: 10.1016/0306-4522(80)90196-7.Google Scholar
Groh, A, Bokor, H, Mease, RA, Plattner, VM, Hangya, B, Stroh, A, Deschênes, M, Acsády, L. (2014) Convergence of cortical and sensory driver inputs on single thalamocortical cells. Cereb Cortex. 24:31673179.Google Scholar
Guido, W, Lu, SM, Sherman, SM. (1992) Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. J Neurophysiol. 68, 21992211. doi:10.1152/jn.1992.68.6.2199.Google Scholar
Guido, W, Weyand, T. (1995) Burst responses in thalamic relay cells of the awake behaving cat. J Neurophysiol. 74:17821786.Google Scholar
Guillery, RW. (1966) A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. J Comp Neurol. 128:2150. doi: 10.1002/cne.901280104.Google Scholar
Guillery, RW. (1995) Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J Anat. 187:583592.Google Scholar
Guillery, RW, Sherman, SM. (2002) Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron. 33:163175. doi: 10.1016/s0896-6273(01)00582-7.Google Scholar
Gutierrez, C, Cox, CL, Rinzel, J, Sherman, SM. (2001) Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus. J Neurosci. 21:10221032.Google Scholar
Harris, JA, Mihalas, S, Hirokawa, KE, Whitesell, JD, Choi, H, Bernard, A, Bohn, P, Caldejon, S, Casal, L, Cho, A, Feiner, A, Feng, D, Gaudreault, N, Gerfen, CR, Graddis, N, Groblewski, PA, Henry, AM, Ho, A, Howard, R, Knox, JE, Kuan, L, Kuang, X, Lecoq, J, Lesnar, P, Li, Y, Luviano, J, McConoughey, S, Mortrud, MT, Naeemi, M, Ng, L, Oh, SW, Ouellette, B, Shen, E, Sorensen, SA, Wakeman, W, Wang, Q, Wang, Y, Williford, A, Phillips, JW, Jones, AR, Koch, C, Zeng, H. (2019) Hierarchical organization of cortical and thalamic connectivity. Nature. 575:195202. doi: 10.1038/s41586-019-1716-z.Google Scholar
Hashikawa, T, Rausell, E, Molinari, M, Jones, EG. (1991) Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: differential distribution and cortical layer specific projections. Brain Res. 544:335341. doi: 10.1016/0006-8993(91)90076-8.Google Scholar
Hendry, SH, Yoshioka, T. (1994) A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science. 264:575577.Google Scholar
Herkenham, M. (1978) The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J Comp Neurol. 177:589610.CrossRefGoogle ScholarPubMed
Herkenham, M. (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol. 183:487517.Google Scholar
Herkenham, M. (1980) Laminar organization of thalamic projections to the rat neocortex. Science. 207:532535.Google Scholar
Herkenham, M. (1986) New perspectives on the organization and evolution of nonspecific thalamocortical projections. In Jones, EG (ed.), Cerebral Cortex, Vol 5. New York: Plenum Press, 1985, pp. 403445.Google Scholar
Houser, CR, Vaughn, JE, Barber, RP, Roberts, E. (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res. 200:341354.Google Scholar
Huang, CL, Winer, JA. (2000) Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J Comp Neurol. 427:302331. doi: 10.1002/1096-9861(20001113)427:2<302::aid-cne10>3.0.co;2-j.Google Scholar
Huguenard, JR. (1996) Low-threshold calcium currents in central nervous system neurons. Ann Rev Physiol. 58:329348. doi:10.1146/annurev.ph.58.030196.001553Google Scholar
Humphrey, AL, Sur, M, Uhlrich, DJ, Sherman, SM. (1985) Termination patterns of individual X- and Y-cell axons in the visual cortex of the cat: projections to area 18, to the 17/18 border region, and to both areas 17 and 18. J Comp Neurol. 233:190212. doi: 10.1002/cne.902330204.Google Scholar
Jager, P, Moore, G, Calpin, P, Durmishi, X, Salgarella, I, Menage, L, Kita, Y, Wang, Y, Kim, DW, Blackshaw, S, Schultz, SR, Brickley, S, Shimogori, T, Delogu, A. (2021) Dual midbrain and forebrain origins of thalamic inhibitory interneurons. eLife. Feb 1;10:e59272. doi: 10.7554/eLife.59272.Google Scholar
Jahnsen, H, Llinás, R. (1984a) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 349:205226. doi: 10.1113/jphysiol.1984.sp015153.Google Scholar
Jahnsen, H, Llinás, R. (1984b) Voltage-dependent burst-to-tonic switching of thalamic cell activity: An in vitro study. Arch Ital Biol. 122:7382.Google Scholar
Jaramillo, J, Mejias, JF, Wang, X-J. (2019) Engagement of pulvinocortical feedforward and feedback pathways in cognitive computations. Neuron. 101:321336. doi: 10.1016/j.neuron.2018.11.023.Google Scholar
Jhangiani-Jashanmal, IT, Yamamoto, R, Gungor, NZ, Paré, D. (2016) Electroresponsive properties of rat central medial thalamic neurons. J Neurophysiol. 115:15331541. doi: 10.1152/jn.00982.2015.Google Scholar
Jones, EG. (1998) Viewpoint: the core and matrix of thalamic organization. Neuroscience. 85:331345.Google Scholar
Jones, EG. (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 24, 595601.Google Scholar
Jones, EG. (2007a) Thalamic neurons, synaptic organization, and functional properties. In The Thalamus, 2nd ed., Vol. 1. Cambridge: Cambridge University Press, Ch. 4, pp. 171317.Google Scholar
Jones, EG. (2007b) The chemistry of the thalamus. In The Thalamus, 2nd ed., Vol. 1. Cambridge: Cambridge University Press, Ch. 5, pp. 318478.Google Scholar
Jones, EG, Burton, H. (1976) Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates. J Comp Neurol. 168: 197247.Google Scholar
Jones, EG, Leavitt, RY. (1974) Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J Comp Neurol. 154:349377. doi: 10.1002/cne.901540402.Google Scholar
Kageyama, GH, Wong-Riley, MT. (1984) The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat, and monkey, with particular reference to retinal mosaics and ON/OFF-center visual channels. J Neurosci. 4:24452459. doi: 10.1523/JNEUROSCI.04-10-02445.1984.Google Scholar
Kaufman, EF, Rosenquist, AC. (1985) Efferent projections of the thalamic intralaminar nuclei in the cat. Brain Res. 335, 257279.Google Scholar
Kerschensteiner, D, Guido, W. (2017) Organization of the dorsal lateral geniculate nucleus in the mouse. Vis Neurosci. Jan;34:E008. doi: 10.1017/S0952523817000062.Google Scholar
Killackey, H, Ebner, F. (1972) Two different types of thalamocortical projections to a single cortical area in mammals. Brain Behav Evol. 6:141–69.Google Scholar
Killackey, H, Ebner, F. (1973) Convergent projection of three separate thalamic nuclei on to a single cortical area. Science. 179, 283285.Google Scholar
Kim, EJ, Zhang, Z, Huang, L, Ito-Cole, T, Jacobs, MW, Juavinett, AL, Senturk, G, Hu, M, Ku, M, Ecker, JR, Callaway, EM. (2020) Extraction of distinct neuronal cell types from within a genetically continuous population. Neuron. 107:274282. doi: 10.1016/j.neuron.2020.04.018.CrossRefGoogle ScholarPubMed
Kirouac, GJ. (2015) Placing the paraventricular nucleus of the thalamus within the brain circuits that control behavior. Neurosci Biobehav Rev. 56:315329. doi: 10.1016/j.neubiorev.2015.08.005.Google Scholar
Kuramoto, E, Furuta, T, Nakamura, KC, Unzai, T, Hioki, H, Kaneko, T. (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex. 19:20652077.Google Scholar
Kuramoto, E, Iwai, H, Yamanaka, A, Ohno, S, Seki, H, Tanaka, YR, Furuta, T, Hioki, H, Goto, T. (2017) Dorsal and ventral parts of thalamic nucleus submedius project to different areas of rat orbitofrontal cortex: A single neuron-tracing study using virus vectors. J Comp Neurol. 525:38213839. doi: 10.1002/cne.24306. Epub 2017.Google Scholar
Kuramoto, E, Ohno, S, Furuta, T, Unzai, T, Tanaka, YR, Hioki, H, Kaneko, T. (2015) Ventral medial nucleus neurons send thalamocortical afferents more widely and more preferentially to layer 1 than neurons of the ventral anterior–ventral lateral nuclear complex in the rat. Cereb Cortex. 25:221235.Google Scholar
Kuramoto, E, Pan, S, Furuta, T, Tanaka, YR, Iwai, H, Yamanaka, A, Ohno, S, Kaneko, T, Goto, T, Hioki, H. (2017) Individual mediodorsal thalamic neurons project to multiple areas of the rat prefrontal cortex: a single neuron-tracing study using virus vectors. J Comp Neurol. 525:166185. doi: 10.1002/cne.24054.Google Scholar
Lacey, CJ, Bolam, JP, Magill, PJ. (2007) Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci. 27:43744384. doi: 10.1523/JNEUROSCI.5519-06.2007.Google Scholar
Lanciego, JL, Gonzalo, N, Castle, M, Sanchez-Escobar, C, Aymerich, MS, Obeso, JA. (2004) Thalamic innervation of striatal and subthalamic neurons projecting to the rat entopeduncular nucleus. Eur J Neurosci. 19:12671277. doi: 10.1111/j.1460-9568.2004.03244.x.Google Scholar
Land, PW, Simons, DJ. (1985) Metabolic and structural correlates of the vibrissae representation in the thalamus of the adult rat. Neurosci Lett. 60:319324. doi: 10.1016/0304-3940(85)90597-x.Google Scholar
Landisman, CE, Connors, BW. (2007) VPM and PoM nuclei of the rat somatosensory thalamus: Intrinsic neuronal properties and corticothalamic feedback. Cereb Cortex. 17:28532865. https://doi.org/10.1093/cercor/bhm025Google Scholar
Leresche, N, Lightowler, S, Soltesz, I, Jassik-Gerschenfeld, D, Crunelli, V. (1991) Low-frequency oscillatory activities intrinsic to rat and cat thalamocortical cells. J Physiol. 441:155174.Google Scholar
LeVay, S, Gilbert, CD. (1976) Laminar patterns of geniculocortical projection in the cat. Brain Res. 113:119.Google Scholar
Leventhal, AG. (1979) Evidence that the different classes of relay cells of the cat’s lateral geniculate nucleus terminate in different layers of the striate cortex. Exp Brain Res. 37:349372. doi: 10.1007/BF00237719.Google Scholar
Li, J, Bickford, ME, Guido, W. (2003) Distinct firing properties of higher order thalamic relay neurons. J Neurophysiol. 90:291299. doi: 10.1152/jn.01163.2002Google Scholar
Li, Y, Lopez-Huerta, VG, Adiconis, X, Levandowski, K, Choi, S, Simmons, SK, Arias-Garcia, MA, Guo, B, Yao, AY, Blosser, TR, Wimmer, RD, Aida, T, Atamian, A, Naik, T, Sun, X, Bi, D, Malhotra, D, Hession, CC, Shema, R, Gomes, M, Li, T, Hwang, E, Krol, A, Kowalczyk, M, Peça, J, Pan, G, Halassa, MM, Levin, JZ, Fu, Z, Feng, G. (2020) Distinct subnetworks of the thalamic reticular nucleus. Nature. 583:819824. doi: 10.1038/s41586-020-2504-5.Google Scholar
Llinás, R, Jahnsen, H. (1982) Electrophysiology of mammalian thalamic neurones in vitro. Nature. 297:406408. doi: 10.1038/297406a0.Google Scholar
Llinás, RR Steriade, M. (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol. 95:32973308. doi:10.1152/jn.00166.2006.Google Scholar
López-Bendito, G, Cautinat, A, Sánchez, JA, Bielle, F, Flames, N, Garratt, AN, Talmage, DA, Role, LW, Charnay, P, Marín, O, Garel, S. (2006) Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell. 125:127142. doi: 10.1016/j.cell.2006.01.042.Google Scholar
López-Bendito, G, Molnar, Z. (2003) Thalamocortical development: how are we going to get there? Nat Rev Neurosci. 4:276289. doi:10.1038/nrn1075.Google Scholar
Lorente de No, R. (1938) Cerebral cortex: architecture, intracortical connections, motor projections. In Fulton, J (ed.), Physiology of the nervous system. London: Oxford University Press. pp. 291340.Google Scholar
Lund, JS. (1988) Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci. 11:253288. doi: 10.1146/annurev.ne.11.030188.001345.Google Scholar
Macchi, G, Bentivoglio, M, Minciacchi, D, Molinari, M. (1996) Trends in the anatomical organization and functional significance of the mammalian thalamus. Ital J Neurol Sci. 17:105129. doi: 10.1007/BF02000842.Google Scholar
Macchi, G, Bentivoglio, M, Molinari, M, Minciacchi, D. (1984) The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp Brain Res. 54:225239. doi: 10.1007/BF00236222.Google Scholar
Mandelbaum, G, Taranda, J, Haynes, TM, Hochbaum, DR, Huang, KW, Hyun, M, Umadevi Venkataraju, K, Straub, C, Wang, W, Robertson, K, Osten, P, Sabatini, BL. (2019) Distinct cortical-thalamic-striatal circuits through the parafascicular nucleus. Neuron. 102:636652. doi: 10.1016/j.neuron.2019.02.035.Google Scholar
Martini, FJ, Guillamón-Vivancos, T, Moreno-Juan, V, Valdeolmillos, M, López-Bendito, G. (2021) Spontaneous activity in developing thalamic and cortical sensory networks. Neuron. 109:25192534. doi: 10.1016/j.neuron.2021.06.026.Google Scholar
Minciacchi, D, Bentivoglio, M, Molinari, M, Kultas-Ilinsky, K, Ilinsky, IA, Macchi, G. (1986) Multiple cortical targets of one thalamic nucleus: the projections of the ventral medial nucleus in the cat studied with retrograde tracers. J Comp Neurol. 252:106129.Google Scholar
Mitani, A, Itoh, K, Mizuno, N. (1987) Distribution and size of thalamic neurons projecting to layer I of the auditory cortical fields of the cat compared to those projecting to layer IV. J Comp Neurol. 257:105121.Google Scholar
Molnár, Z, Garel, S, López-Bendito, G, Maness, P, Price, DJ. (2012) Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. Eur J Neurosci. 35:15731585. doi: 10.1111/j.1460-9568.2012.08119.xGoogle Scholar
Monckton, JE, McCormick, DA. (2002) Neuromodulatory role of serotonin in the ferret thalamus. J Neurophysiol. 87:21242136. doi: 10.1152/jn.00650.2001.Google Scholar
Morest, DK. (1964) The neuronal architecture of the medial geniculate body of the cat. J Anat. 98:611630. PMID: 14229992.Google Scholar
Murray, KD, Choudary, PV, Jones, EG. (2007) Nucleus- and cell-specific gene expression in monkey thalamus. Proc Natl Acad Sci USA. 104:1989–1994.Google Scholar
Nagalski, A, Puelles, L, Dabrowski, M, Wegierski, T, Kuznicki, J, Wisniewska, MB. (2016) Molecular anatomy of the thalamic complex and the underlying transcription factors. Brain Struct Funct. 221:24932510. doi: 10.1007/s00429-015-1052-5.Google Scholar
Nakagawa, Y. (2019) Development of the thalamus: From early patterning to regulation of cortical functions. Wiley Interdiscip Rev Dev Biol. Sep;8(5):e345. doi: 10.1002/wdev.345.Google Scholar
Nakamura, H, Hioki, H, Furuta, T, Kaneko, T. (2015) Different cortical projections from three subdivisions of the rat lateral posterior thalamic nucleus: a single-neuron tracing study with viral vectors. Eur J Neurosci. 41:12941310.Google Scholar
Nakamura, KC, Sharott, A, Magill, PJ. (2014) Temporal coupling with cortex distinguishes spontaneous neuronal activities in identified basal ganglia-recipient and cerebellar-recipient zones of the motor thalamus. Cereb Cortex. 24:8197. doi: 10.1093/cercor/bhs287.Google Scholar
Namura, S, Takada, M, Kikuchi, H, Mizuno, N. (1997) Collateral projections of single neurons in the posterior thalamic region to both the temporal cortex and the amygdala: a fluorescent retrograde double-labeling study in the rat. J Comp Neurol. 384:5970.Google Scholar
Noseda, R, Jakubowski, M, Kainz, V, Borsook, D, Burstein, R. (2011) Cortical projections of functionally identified thalamic trigeminovascular neurons: implications for migraine headache and its associated symptoms. J. Neurosci. 31:1420414217.Google Scholar
Noseda, R, Kainz, V, Jakubowski, M, Gooley, JJ, Saper, CB, Digre, K, Burstein, R. (2010) A neural mechanism for exacerbation of headache by light. Nat. Neurosci. 13:239245. doi: 10.1038/nn.2475. Epub 2010 Jan 10.Google Scholar
Nuñez, A, Amzica, F, Steriade, M. (1992) Intrinsic and synaptically generated delta (1–4 Hz) rhythms in dorsal lateral geniculate neurons and their modulation by light-induced fast (30–70 Hz) events. Neuroscience. 51:269284.Google Scholar
Oberlaender, M, Ramirez, A, Bruno, RM. (2012) Sensory experience restructures thalamocortical axons during adulthood. Neuron. 74, 648655.Google Scholar
Oh, SW, Harris, JA, Ng, L, Winslow, B, Cain, N, Mihalas, S, Wang, Q, Lau, C, Kuan, L, Henry, AM, Mortrud, MT, Ouellette, B, Nguyen, TN, Sorensen, SA, Slaughterbeck, CR, Wakeman, W, Li, Y, Feng, D, Ho, A, Nicholas, E, Hirokawa, KE, Bohn, P, Joines, KM, Peng, H, Hawrylycz, MJ, Phillips, JW, Hohmann, JG, Wohnoutka, P, Gerfen, CR, Koch, C, Bernard, A, Dang, C, Jones, AR, Zeng, H. (2014) A mesoscale connectome of the mouse brain. Nature. 508:207214. doi: 10.1038/nature13186.Google Scholar
Ohno, S, Kuramoto, E, Furuta, T, Hioki, H, Tanaka, YR, Fujiyama, F, Sonomura, T, Uemura, M, Sugiyama, K, Kaneko, T. (2012) A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb Cortex. 22: 28402857.Google Scholar
Parent, M, Parent, A. (2005) Single-axon tracing and three-dimensional reconstruction of centre median-parafascicular thalamic neurons in primates. J Comp Neurol. 481:127144. doi: 10.1002/cne.20348.Google Scholar
Pedroarena, C. Llinás, R. (1997) Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons. Proc Natl Acad Sci USA. 94:724728.Google Scholar
Penny, GR, Itoh, K, Diamond, IT. (1982) Cells of different sizes in the ventral nuclei project to different layers of the somatic cortex in the cat. Brain Res. 242:5565. doi: 10.1016/0006-8993(82)90495-4.Google Scholar
Perez-Reyes, E. (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev. 83:117161. doi: 10.1152/physrev.00018.2002.Google Scholar
Phillips, JW, Schulmann, A, Hara, E, Winnubst, J, Liu, C, Valakh, V, Wang, L, Shields, BC, Korff, W, Chandrashekar, J, Lemire, AL, Mensh, B, Dudman, JT, Nelson, SB, Hantman, AW. (2019) A repeated molecular architecture across thalamic pathways. Nat Neurosci. 22:19251935. doi: 10.1038/s41593-019-0483-3.Google Scholar
Pinault, D. (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Meth. 65:113136.Google Scholar
Puelles, L, Rubenstein, JL. (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 26:469476.Google Scholar
Ramón y Cajal, S (1904) Textura del Sistema Nervioso del Hombre y de los Vertebrados. II Parte., Vol. 2. Madrid: Imprenta Nicolás Moya.Google Scholar
Rausell, E, Avendaño, C. (1985) Thalamocortical neurons projecting to superficial and to deep layers in parietal, frontal and prefrontal regions in the cat. Brain Res. 347:159165.Google Scholar
Rausell, E, Bae, CS, Viñuela, A, Huntley, GW, Jones, EG. (1992) Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations. J Neurosci. 12:40884111.Google Scholar
Rausell, E, Jones, EG. (1991) Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map. J Neurosci. 11:210225. doi: 10.1523/JNEUROSCI.11-01-00210.1991.Google Scholar
Real, MA, Dávila, JC, Guirado, S. (2006) Immunohistochemical localization of the vesicular glutamate transporter VGLUT2 in the developing and adult mouse claustrum. J Chem Neuroanat. 31:169177.Google Scholar
Reinagel, P, Godwin, D, Sherman, SM, Koch, C. (1999) Encoding of visual information by LGN bursts. J Neurophysiol. 81:25582569. doi: 10.1152/jn.1999.81.5.2558Google Scholar
Ren, S, Wang, Y, Yue, F, Cheng, X, Dang, R, Qiao, Q, Sun, X, Li, X, Jiang, Q, Yao, J, Qin, H, Wang, G, Liao, X, Gao, D, Xia, J, Zhang, J, Hu, B, Yan, J, Wang, Y, Xu, M, Han, Y, Tang, X, Chen, X, He, C, Hu, Z. (2018) The paraventricular thalamus is a critical thalamic area for wakefulness. Science. 362:429434. doi: 10.1126/science.aat2512.Google Scholar
Rodriguez-Moreno, J, Porrero, C, Rollenhagen, A, Rubio-Teves, M, Casas-Torremocha, D, Alonso-Nanclares, L, Yakoubi, R, Santuy, A, Merchan-Pérez, A, DeFelipe, J, Lübke, JHR, Clascá, F. (2020) Area-specific synapse structure in branched posterior nucleus axons reveals a new level of complexity in thalamocortical networks. J Neurosci. 40:26632679. doi: 10.1523/JNEUROSCI.2886-19.2020.Google Scholar
Rodriguez-Moreno, J, Rollenhagen, A, Arlandis, J, Santuy, A, Merchan-Pérez, A, DeFelipe, J, Lübke, JHR, Clascá, F. (2018) Quantitative 3D ultrastructure of thalamocortical synapses from the “lemniscal” ventral posteromedial nucleus in mouse barrel cortex. Cereb Cortex. 28:31593175. doi: 10.1093/cercor/bhx187.Google Scholar
Rubio-Garrido, P, Pérez-de-Manzo, F, Porrero, C, Galazo, MJ, Clascá, F. (2009) Thalamic input to distal apical dendrites in neocortical layer 1 is massive and highly convergent. Cereb Cortex. 19:23802395. doi: 10.1093/cercor/bhn259.Google Scholar
Sampathkumar, V, Miller-Hansen, A, Sherman, SM, Kasthuri, N. (2021) Integration of signals from different cortical areas in higher order thalamic neurons. Proc Natl Acad Sci USA. 118(30):e2104137118. doi: 10.1073/pnas.2104137118.Google Scholar
Scheibel, ME, Scheibel, AB. (1966) The organization of the ventral anterior nucleus of the thalamus. A Golgi study. Brain Res. 1:250268. doi: 10.1016/0006-8993(66)90091-6.Google Scholar
Sherman, SM. (2001a) A wake-up call from the thalamus. Nat Neurosci. 4:344346. doi: 10.1038/85973.Google Scholar
Sherman, SM. (2001b) Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24:122126. doi: 10.1016/s0166-2236(00)01714-8.Google Scholar
Sheroziya, M, Timofeev, I. (2014) Global intracellular slow-wave dynamics of the thalamocortical system. J Neurosci. 34:88758893. doi: 10.1523/JNEUROSCI.4460-13.2014.Google Scholar
Shi, W, Xianyu, A, Han, Z, Tang, X, Li, Z, Zhong, H, Mao, T, Huang, K, Shi, SH. (2017) Ontogenetic establishment of order-specific nuclear organization in the mammalian thalamus. Nat Neurosci. 20:516528. doi: 10.1038/nn.4519.CrossRefGoogle ScholarPubMed
Shibata, H. (1993a) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol. 337:431445. doi: 10.1002/cne.903370307.Google Scholar
Shibata, H. (1993b) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol. 330:533542. doi: 10.1002/cne.903300409.Google Scholar
Slézia, A, Hangya, B, Ulbert, I, Acsády, L. (2011) Phase advancement and nucleus-specific timing of thalamocortical activity during slow cortical oscillation. J Neurosci. 31:607617. doi: 10.1523/JNEUROSCI.3375-10.2011.CrossRefGoogle ScholarPubMed
Smith, PH, Bartlett, EL, Kowalkowski, A. (2006) Unique combination of anatomy and physiology in cells of the rat paralaminar thalamic nuclei adjacent to the medial geniculate body. J Comp Neurol. 496:314334. doi: 10.1002/cne.20913.Google Scholar
Smith, Y, Galvan, A, Ellender, TJ, Doig, N, Villalba, RM, Huerta-Ocampo, I, Wichmann, T, Bolam, JP. (2014) The thalamostriatal system in normal and diseased states. Front Syst Neurosci. Jan 30;8:5. doi: 10.3389/fnsys.2014.00005.Google Scholar
Stanford, LR, Friedlander, MJ, Sherman, SM. (1983) Morphological and physiological properties of geniculate W-cells of the cat: a comparison with X- and Y-cells. J Neurophysiol. 50:582608. doi: 10.1152/jn.1983.50.3.582.Google Scholar
Swadlow, HA, Gusev, AG. (2001) The impact of “bursting” thalamic impulses at a neocortical synapse. Nat Neurosci. 4:402408. doi: 10.1038/86054.Google Scholar
Turner, JP, Anderson, CM, Williams, SR, Crunelli, V. (1997) Morphology and membrane properties of neurones in the cat ventrobasal thalamus in vitro. J Physiol. 505:707726.Google Scholar
Turner, JP, Leresche, N, Guyon, A, Soltesz, I, Crunelli, V. (1994) Sensory input and burst firing output of rat and cat thalamocortical cells: the role of NMDA and non-NMDA receptors. J Physiol. 480:281295.Google Scholar
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. 27:11641181. doi: 10.1093/cercor/bhv295.Google Scholar
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. 39:107140. doi: 10.1016/s0165-0173(02)00181-9.Google Scholar
Van Groen, T, Kadish, I, Wyss, JM. (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Brain Res Rev. 30:126. doi: 10.1016/s0165-0173(99)00006-5.Google Scholar
Van Groen, T, Wyss, JM. (1995) Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J Comp Neurol. 358:584604. doi: 10.1002/cne.903580411.Google Scholar
Vanderhaeghen, P, Polleux, F. (2004) Developmental mechanisms patterning thalamocortical projections: intrinsic, extrinsic and in between. Trends Neurosci. 27:384391.Google Scholar
Varela, C, Sherman, SM. (2009) Differences in response to serotonergic activation between first and higher order thalamic nuclei. Cereb Cortex. 19:17761786. doi: 10.1093/cercor/bhn208.Google Scholar
Vertes, RP, Hoover, WB. (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol. 508:212237. doi: 10.1002/cne.21679.Google Scholar
Vertes, RP, Hoover, WB, Do Valle, AC, Sherman, A, Rodriguez, JJ. (2006) Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J Comp Neurol. 499:768–96. doi: 10.1002/cne.21135.Google Scholar
Vertes, RP, Hoover, WB, Rodriguez, JJ. (2012) Projections of the central medial nucleus of the thalamus in the rat: node in cortical, striatal and limbic forebrain circuitry. Neuroscience. 219:120136. doi: 10.1016/j.neuroscience.2012.04.067.Google Scholar
Vue, TY, Aaker, J, Taniguchi, A, Kazemzadeh, C, Skidmore, JM, Martin, DM, Martin, JF, Treier, M, Nakagawa, Y. (2007) Characterization of progenitor domains in the developing mouse thalamus. J Comp Neurol. 505:7391. doi: 10.1002/cne.21467.Google Scholar
Wang, Q, Ding, SL, Li, Y, Royall, J, Feng, D, Lesnar, P, Graddis, N, Naeemi, M, Facer, B, Ho, A, Dolbeare, T, Blanchard, B, Dee, N, Wakeman, W, Hirokawa, KE, Szafer, A, Sunkin, SM, Oh, SW, Bernard, A, Phillips, JW, Hawrylycz, M, Koch, C, Zeng, H, Harris, JA, Ng, L. (2020) The Allen mouse brain common coordinate framework: A 3D reference atlas. Cell. 181:936–953.e20. doi: 10.1016/j.cell.2020.04.007.Google Scholar
Wang, X, Wei, Y, Vaingankar, V, Wang, Q, Koepsell, K, Sommer, FT, Hirsch, JA. (2007) Feedforward excitation and inhibition evoke dual modes of firing in the cat’s visual thalamus during naturalistic viewing. Neuron. 55:465478. doi: 10.1016/j.neuron.2007.06.039.Google Scholar
Wei, H, Bonjean, M, Petry, HM, Sejnowski, TJ, Bickford, ME. (2011) Thalamic burst firing propensity: A comparison of the dorsal lateral geniculate and pulvinar nuclei in the tree shrew. J Neurosci. 31:1728717299. doi: 10.1523/JNEUROSCI.6431-10.2011Google Scholar
Whitmire, CJ., Waiblinger, C, Schwarz, C, Stanley, GB. (2016) Information coding through adaptive gating of synchronized thalamic bursting. Cell Rep. 14:795807. doi: 10.1016/j.celrep.2015.12.068.Google Scholar
Winnubst, J, Bas, E, Ferreira, TA, Wu, Z, Economo, MN, Edson, P, Arthur, BJ, Bruns, C, Rokicki, K, Schauder, D, Olbris, DJ, Murphy, SD, Ackerman, DG, Arshadi, C, Baldwin, P, Blake, R, Elsayed, A, Hasan, M, Ramirez, D, Dos Santos, B, Weldon, M, Zafar, A, Dudman, JT, Gerfen, CR, Hantman, AW, Korff, W, Sternson, SM, Spruston, N, Svoboda, K, Chandrashekar, J. (2019) Reconstruction of 1,000 projection neurons reveals new cell types and organization of long-range connectivity in the mouse brain. Cell. 179:268281. doi: 10.1016/j.cell.2019.07.042.Google Scholar
Winnubst, J, Spruston, N, Harris, JA. (2020) Linking axon morphology to gene expression: a strategy for neuronal cell-type classification. Curr Opin Neurobiol. 65:7076. doi: 10.1016/j.conb.2020.10.006.Google Scholar
Wong, SZH, Scott, EP, Mu, W, Guo, X, Borgenheimer, E, Freeman, M, Ming, G, Wu, QF, Song, H, Nakagawa, Y. (2018) In vivo clonal analysis reveals spatiotemporal regulation of thalamic nucleogenesis. PLoS Biol. 16(4):e2005211. doi: 10.1371/journal.pbio.2005211.Google Scholar
Wouterlood, FG, Saldana, E, Witter, MP. (1990) Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer phaseolus vulgaris-leucoagglutinin. J Comp Neurol. 296:179203. doi: 10.1002/cne.Google Scholar
Yasui, Y, Itoh, K, Sugimoto, T, Kaneko, T, Mizuno, N. (1987) Thalamocortical and thalamo-amygdaloid projections from the parvicellular division of the posteromedial ventral nucleus in the cat. J Comp Neurol. 257:253268. doi: 10.1002/cne.902570210.Google Scholar
Yen, CT, Conley, M, Jones, EG. (1985) Morphological and functional types of neurons in cat ventral posterior thalamic nucleus. J Neurosci. 5:13161338.Google Scholar

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