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Viewpoint: the core and matrix of thalamic organization
Abstract
The integration of the whole cerebral cortex and thalamus during forebrain activities that underlie different states of consciousness, requires pathways for the dispersion of thalamic activity across many cortical areas. Past theories have relied on the intralaminar nuclei as the sources of diffuse thalamocortical projections that could facilitate spread of activity across the cortex. A case is made for the presence of a matrix of superficially-projecting cells, not confined to the intralaminar nuclei but extending throughout the whole thalamus. These cells are distinguished by immunoreactivity for the calcium-binding protein, D28K calbindin, are found in all thalamic nuclei of primates and have increased numbers in some nuclei. They project to superficial layers of the cerebral cortex over relatively wide areas, unconstrained by architectonic boundaries. They generally receive subcortical inputs that lack the topographic order and physiological precision of the principal sensory pathways. Superimposed upon the matrix in certain nuclei only, is a core of cells distinguished by immunoreactivity for another calcium-binding protein, parvalbumin, These project in highly ordered fashion to middle layers of the cortex in an area-specific manner. They are innervated by subcortical inputs that are topographically precise and have readily identifiable physiological properties. The parvalbumin cells form the basis for sensory and other inputs that are to be used as a basis for perception. The calbindin cells, especially when recruited by corticothalamic connections, can form a basis for the engagement of multiple cortical areas and thalamic nuclei that is essential for the binding of multiple aspects of sensory experience into a single framework of consciousness.
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“Matrix cells are distributed widely over the nuclei of the dorsal thalamus and send thalamocortical axons that terminate principally in the superficial layers of the cortex [36,37].”
From Cerebral hierarchies: predictive processing, precision and the pulvinar (2015) · cites this paper as [37]
In the citing paper
“The specific observations from our data are mostly consistent (with a few additions) with extensive previous studies in rats and the fewer number of studies in mice (Extended Data Fig. 10) as well as with studies in other mammalian species37–39, providing a comprehensive and unifying view of mouse cortico-thalamic connections for the first time.”
From A mesoscale connectome of the mouse brain (2014) · cites this paper as [38]
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“For instance, koniocellular cells of the lateral geniculate nucleus of monkeys, cells that stain for calbindin, are identi fi ed as matrix (Jones, 1998).”
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“Considering the distinction between ‘matrix’ and ‘core’ cells proposed by Jones 116,122,123 is particularly relevant for this discourse.”
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LaBerge, D., & Kasevich, R. S. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00037 · Cited by 14
“Thalamic neurons that project to the cortex are of two main types, called “core” neurons and “matrix” neurons, which are distinguished by their immunoreactivity for the calbindin calcium-binding protein and the parvalbumin calcium-binding protein, respectively (Jones, 1998, 2007).”
BackgroundHämäläinen, M., Huang, M., & Bowyer, S. M. (2020) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2020.02.001 · Cited by 12
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“The thalamus acts as a sensory relay by directing peripherical information to the cortex and as an integrative hub for cortical representations by mediating cortico-cortical communication (Hwang et al., 2017; Jones, 1998; Malekmohammadi et al., 2015; Sherman and Guillery, 2013).”
BackgroundThe Reticular Formation and Some Related Nuclei
ten Donkelaar, H. J. (2011) · Springer eBooks · doi:10.1007/978-3-642-19134-3_5 · Cited by 12
Leitch, B. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189821 · Cited by 12
“Corticothalamic (CT) axonal projections from pyramidal cells in layers 5/6 of the cortex make excitatory connections onto relay neurons in the ventroposterior (VP) thalamus, which in turn send thalamocortical (TC) axonal projections back to cortical neurons in layer 4 of the cortex [63–65].”
BackgroundVentromedial Thalamus-Projecting DCN Neurons Modulate Associative Sensorimotor Responses in Mice
Zhang, J., Chen, H., Zhang, L.-B., Li, R.-R., Wang, B., Zhang, Q.-H., Tong, L.-X., Zhang, W.-W., Yao, Z.-X., & Hu, B. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-021-00810-9 · Cited by 11
“Unlike the VL, there are abundant calbindin neurons in the Vm [20, 21].”
BackgroundBrief Introduction to Electroencephalography
Proekt, A. (2018) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2018.02.009 · Cited by 11
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Neural representations of the sense of self
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“Note that primary neocortical input comes from the thalamus, terminating in layer 4 (Jones, 1998).”
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Adams, P. R., & Cox, K. J. A. (2002) · Neurocomputing · doi:10.1016/s0925-2312(01)00591-4 · Cited by 11
“Another possibility is that the relevent K cells feedback to a separate population of relay cells (perhaps the “matrix” cells [18]) that in turn innervate the apical tufts of cortical pyramidal cells, where they would facilitate spike backpropagation.”
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“Comparison of the projections in different taxa suggests that the diffuse connections of the surrounding areas of auditory nuclei are plesiomorphic [Huffman and Henson, 1990; Belekhova et al., 2002; Zeng et al., 2004].”
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Phillips, J. W., Schulmann, A., Hara, E., Liu, C., Wang, L., Shields, B. C., Korff, W. L., Lemire, A. L., Dudman, J. T., Nelson, S. B., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/241315 · Cited by 11
Optogenetic activation of visual thalamus generates artificial visual percepts
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The Somatosensory Thalamus and Associated Pathways
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Yamakawa, H. (2020) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2020.00074 · Cited by 8
“Typically, thalamic core neurons are most strongly associated with sensory relays, such as the lateral geniculate nucleus (Jones, 1998; Clascá et al., 2012).”
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Kim, H. R., Hong, S. Z., & Fiorillo, C. D. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00428 · Cited by 9
“An apparently related distinction, based on morphology and axonal targets, has been made between C-type and M-type TC neurons (as well as less common subtypes), which predominate in lower and higher thalamic nuclei, respectively (Jones, 1998; Clascá et al., 2012).”
BackgroundBelekhova, M., Chudinova, T. V., Rio, J., Tostivint, H., Vesselkin, N., & Kenigfest, N. (2016) · Brain Research · doi:10.1016/j.brainres.2015.11.037 · Cited by 15
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“This division may also be reflected in the core–matrix organization principle: calbindin-immunoreactive (matrix) thalamocortical cells project to the superficial layers and receive spatially diffuse input, whereas parvalbumin-immunoreactive (core) cells target the middle layers and receive more specific input [212].”
BackgroundThe inevitable inequality of cortical columns
Barbas, H., Zikopoulos, B., & John, Y. J. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.921468 · Cited by 9
“A core thalamic system originates in neurons labeled by the calcium binding protein parvalbumin (PV), which are excitatory in the thalamus (unlike the cortex), and project focally to the middle cortical layers (Jones, 1998).”
BackgroundChudinova, T. V., Belekhova, M. G., Tostivint, H., Ward, R. M., Rio, J. P., & Kenigfest, N. B. (2012) · Brain Research · doi:10.1016/j.brainres.2012.07.022 · Cited by 9
“PV is inherent to fast-firing projection neurons in centers of the lemniscal pathway, whereas CB is predominantly expressed in projection neurons belonging to the extralemniscal pathway (Celio, 1990; Baimbridge et al., 1992; Braun and Piepenstock, 1993; Jones, 1998).”
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Belekhova, M. G., Kenigfest, N. B., Mn, M., Rio, J. P., & Repérant, J. (2003) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1023/b:joey.0000023484.49460.c7 · Cited by 9
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“How could delta oscillations be reset to 448 their low-excitability phase? A potential candidate is the deep FS resetter circuit [23], 449 which thalamus matrix cells could activate via projections to infragranular FS cells, or 450 via projections to the apical dendrites of L6 CT cells in L1 [29,35,36], which would in…”
BackgroundPerinatal development of structural thalamocortical connectivity
Oldham, S., Sina Mansour, L., & Ball, G. (2024) · Imaging Neuroscience · doi:10.1162/imag_a_00418 · Cited by 7
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“1992; Jones and Hendry 1989; Jones 1998; Hof et al.”
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“117,118 Most of the lemniscal projections originate from the ventral nucleus of the MGB and they forward stimulus-specific information to the primary auditory cortex (A1).”
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“The second obvious PV-stained fibers were those present near the somatosensory cortex, presumably originating form somatosensory thalamus.(20,33,34) These fibers can be easily separated from OR based on density of axonal cross sections (Figure 6, dashed line in D).”
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“Thus, the mechanism proposed here affords powerful control over inputs to neocortical and non-neocortical regions connected with the thalamus (Jones, 1998; Martel and Galvan, 2022).”
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Organization of the central pain pathways
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“…axons that terminate in the superficial layers of the 381 primary sensory cortex with potentially closer proximity to the anode depending on the 382 individuals anatomy regarding the folding of the postcentral gyrus (Jones, 1998; Tommerdahl 383 et al., 2005a; Tommerdahl et al., 2010).”
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“those that are CB+ and more diffuse (“core” and “matrix,” respectively [34]), although this may hold for only a subdivision of thalamic nuclei.”
BackgroundYazdanbakhsh, A., Barbas, H., & Zikopoulos, B. (2023) · Network Neuroscience · doi:10.1162/netn_a_00311 · Cited by 6
“However, in mammals two anatomically and functionally distinct TC circuits can be identified, the ‘core’ and the ‘matrix’ loops (Jones, 1998; Müller et al., 2020; Rovo et al., 2012; Zikopoulos and Barbas, 2007a), and it is not clear how spindle activity and associated functions are regulated by…”
BackgroundInfluentialAudiovisual Integration in Nonhuman Primates
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Self-citationRevisiting the purpose of the thalamus: anatomically sub-cortical but functionally supra-cortical?
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“In recent years, research on the role of thalamocortical circuits in memory consolidation has attracted significant attention [362], [363].”
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“Specifically, Layer IV is associated with receiving feedforward signal from Layer III of lower cortical areas or from the thalamus (14, 15).”
BackgroundClascá, F. (2023) · Oxford University Press eBooks · doi:10.1093/med/9780197676158.003.0011 · Cited by 3
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“5 ), in which may correspond to afferent fibers from the spinal trigeminal and spinothalamic tracts (Jones 1998).”
InfluentialBelekhova, M. G., Kenigfest, N. B., & Chmykhova, N. M. (2020) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093020040018 · Cited by 4
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“Specifically, Layer IV and to a lesser extent Layer V/VI are commonly associated with receiving feedforward drive from Layer III of lower cortical areas or from the thalamus (Jones, 1998; Constantinople and Bruno, 2013).”
BackgroundPark, S., Haak, K. V., Oldham, S., Cho, H., Byeon, K., Park, B., Thomson, P., Chen, H., Gao, W., Xu, T., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.11.584415 · Cited by 4
“This differentiation may reflect distinct patterns of underlying thalamic projections based on the relative density of ‘core’ and ‘matrix’ cells 10,40 .”
BackgroundZhao, Y., Kouvaros, S., Schneider, N. A., Krall, R. F., Lam, S., Arnold, M. P., Williamson, R. S., & Tzounopoulos, T. (2025) · Science Advances · doi:10.1126/sciadv.adx9737 · Cited by 4
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“65,66 A recent EEG study in SZ has indeed documented a generalized slowing of rhythmic activity, supporting the applicability of this hypothesis in SZ pathophysiology.”
Chapter 8 Ascending nociceptive pathways
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“…thalamocortical interactions in layer I are assumed to be a key substrate for the synchronization of large ensembles of neurons across extensive cortical territories, and have been associated with changes in states of consciousness (Llinás and Ribary, 1993; Steriade et al., 1997; Jones, 1998).”
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“This contrast recalls the distinction of thalamocortical matrix or core terminations (respectively, layer 1 vs. layer 4 targeting; Jones, 1998), although pulvinocortical arborizations are often multil-aminar(Rocklandetal.,1999).”
BackgroundNuclei and tracts in the thalamus of crocodiles
Pritz, M. B. (2024) · The Journal of Comparative Neurology · doi:10.1002/cne.25595 · Cited by 3
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Budinger, E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-805408-6.00022-1 · Cited by 3
Neural Phase Transitions That Made Us Mammals
Treves, A. (2004) · Lecture notes in computer science · doi:10.1007/978-3-540-27862-7_3 · Cited by 4
Identification of male-biased gene: Parvalbumin in song control nuclei of the Bengalese finch
Sun, L., Wang, R., Zeng, S., Geng, Z., Zhang, X., & Zuo, M. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.05.003 · Cited by 3
Chudinova, T. V., Kenigfest, N. B., & Belekhova, M. G. (2010) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093010060113 · Cited by 3
Metabolic activity of the thalamic and telencephalic auditory centers of reptiles
Belekhova, M. G., Chudinova, T. V., Kenigfest, N. B., & Vesselkin, N. P. (2007) · Doklady Biological Sciences · doi:10.1134/s0012496607050018 · Cited by 3
Xi, C., Chen, Q., Zeng, S., Lin, Y., Huang, Y., Liu, Y., Zhang, X., & Zuo, M. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22646 · Cited by 3
Belekhova, M. G., Kenigfest, N. B., & Chudinova, T. V. (2012) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093012030097 · Cited by 3
Jones, S. R. (2011) · Neuromethods · doi:10.1007/7657_2011_16 · Cited by 3
Belekhova, M. G., Kenigfest, N. B., Chudinova, T. V., & Vesselkin, N. P. (2006) · Doklady Biological Sciences · doi:10.1134/s0012496606060196 · Cited by 3
Tosi, Z., & Beggs, J. M. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1706.00133 · Cited by 4
“ded to demonstrate where in the overarching distribution of synaptic strengths (A-C) are sampled from. F) The motif key. receive significant amounts of input from thalamus \core" or C-type cells [70] and send a great deal of outputs to layers II/III [9,15{17]. This thalamus →Layer IV →Layers II/III pathway has be…”
BackgroundVerner, R., Banks, M. I., & Bartlett, E. L. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/213272 · Cited by 3
Funk, C. M., Putnam, M. C., & Gazzaniga, M. S. (2009) · Wiley eBooks · doi:10.1002/9780470478509.neubb001026 · Cited by 3
Propofol Disrupts the Functional Core-Matrix Architecture of the Thalamus in HumansPreprint
Huang, Z., Mashour, G. A., & Hudetz, A. G. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.23.576934 · Cited by 3
The Integrative Brain: Functional Units in Predictive Processing
Phillips, M. C. L. (2025) · Journal of Integrative Neuroscience · doi:10.31083/jin39640 · Cited by 4
“Both circuits involve “driver” and “modulator” inputs [75], as well as core and matrix neuron outputs [71].”
Spike Timing and Thalamocortical Interactions
Usrey, W. M., & Sherman, S. M. (2021) · Oxford University Press eBooks · doi:10.1093/med/9780197503874.003.0010 · Cited by 2
Tapia‐González, S., & DeFelipe, J. (2023) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2023.1210502 · Cited by 2
“A variety of CBPs have been shown to be present in particular subpopulations of neurons in multiple functional systems of the vertebrate nervous system (Celio, 1990; Baimbridge et al., 1992; Jones, 1998; Alpar et al., 2012; Gati et al., 2014).”
BackgroundThalamic Contributions to Multisensory Convergence and Processing
Barczak, A., O’Connell, M. N., & Schroeder, C. E. (2023) · Oxford University Press eBooks · doi:10.1093/med/9780197676158.003.0030 · Cited by 1
Bhagwandin, A., Molnár, Z., Bertelsen, M. F., Karlsson, K. Æ., Alagaili, A. N., Bennett, N. C., Hof, P. R., Kaswera‐Kyamakya, C., Gilissen, E., Jayakumar, J., et al. (2024) · The Journal of Comparative Neurology · doi:10.1002/cne.25652 · Cited by 2
“Despite this, the core and matrix thalamocortical projections as outlined by Jones (1998) are likely to be the patterns most commonly observed across mammals.”
InfluentialAntipova, V., Heimes, D., Seidel, K., Schulz, J., Schmitt, O., Holzmann, C., Rolfs, A., Bidmon, H. J., Román, E. G. D. S., Huesgen, P. F., et al. (2024) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2024.1430790 · Cited by 2
“Resolution: 30 μ m per pixel. cortical pyramidal neurons projecting locally or to disseminated other cortical areas, thalamus, caudate putamen, brainstem, and spinal cord (White and Keller, 1989), as well as thalamocortical and corticothalamic projections (Caviness and Frost, 1980; Jones, 1998).”
BackgroundKenigfest, N. B., Tostivint, H., Quan, F. B., Belekhova, M. G., & Vesselkin, N. P. (2013) · Doklady Biological Sciences · doi:10.1134/s0012496613060045 · Cited by 2
Huang, Y., Zhang, J., Xi, C., Zeng, S., Zhang, X., & Zuo, M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.12.026 · Cited by 2
Casagrande, V. A., Shostak, Y., Wenger, A., & Mavity‐Hudson, J. (2014) · Eye and Brain · doi:10.2147/eb.s51817 · Cited by 2
“From the proposed wider distribution of matrix axons, Jones 16 argued that while the core provides topographically precise sensory messages, axons forming the matrix might provide a means of binding messages together.”
InfluentialRôle des canaux calciques de type T dans les douleurs neuropathiques
Lesport, P., & Bourinet, E. (2016) · Douleur et Analgésie · doi:10.1007/s11724-016-0481-4 · Cited by 2
Belekhova, M. G., Chudinova, T. V., & Kenigfest, N. B. (2016) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s1234567816060070 · Cited by 2
“Inter-species variability in the level of PV- and CBir neurons in the central, lemniscal, regions occurs in the homological thalamic auditory centers in mammals (MGB) [1, 5, 6] and reptiles (nucleus”
InfluentialChangeux, J. (2007) · Elsevier eBooks · doi:10.1016/b978-044452977-0/50007-3 · Cited by 2
Metadata
- Authors
- Jones, E. G.
- Affiliations
- University of California, Irvine (US)
- Corresponding author
- Jones, E.G
- ORCID
- Jones, E.G
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1998-04
- Volume
- 85
- Issue
- 2
- Pages
- 331-345
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2054508155
- Cited by
- 504
- References
- 73
- Citations by year
- 2026: 15 · 2025: 21 · 2024: 23 · 2023: 25 · 2022: 13 · 2021: 38 · 2020: 23 · 2019: 24 · 2018: 19 · 2017: 21 · 2016: 17 · 2015: 23 · 2014: 20 · 2013: 10 · 2012: 14
- FWCI
- 1.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ns022317-08)
- National Institute of Neurological Disorders and Stroke (NS-22317, NS21377, R01NS021377)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- thalamus, thalamocortical connections, intralaminar nuclei, calbindin, parvalbumin, calcium-binding proteins, cortical layers, corticothalamic connections, consciousness, primates
- MeSH terms
- Animals, Cerebral Cortex, Humans, Neural Pathways, Neurons, Thalamus
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