Cited by 504Neural dynamics and brain functionVisual perception and processing mechanismsNeuroscience and Neuropharmacology Research

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Viewpoint: the core and matrix of thalamic organization

Jones, E.G·1998·Neuroscience

DOI 10.1016/s0306-4522(97)00581-2

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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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Systematic expression analysis of Hox genes at adulthood reveals novel patterns in the central nervous system
Hutlet, B., Theys, N., Coste, C., Ahn, M., Doshishti-Agolli, K., Lizen, B., & Gofflot, F. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0965-8 · Cited by 56
“The thalamus receives input from touch, auditory and visual pathways, among others, and sends fibres to the cerebral cortex (Jones 1998).”
Background
Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex
Brennan, E. K. W., Jedrasiak‐Cape, I., Kailasa, S., Rice, S. P., Sudhakar, S., & Ahmed, O. J. (2021) · eLife · doi:10.7554/elife.62207 · Cited by 58
Central Thalamic Deep‐Brain Stimulation in the Severely Injured Brain
Schiff, N. D. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.04123.x · Cited by 55
Mesocircuit mechanisms in the diagnosis and treatment of disorders of consciousness
Schiff, N. D. (2022) · La Presse Médicale · doi:10.1016/j.lpm.2022.104161 · Cited by 56
Thalamocortical dysrhythmia syndrome: MEG imaging of neuropathic pain
Schulman, J. J., RAMIREZ, R. R., Zonenshayn, M., Ribary, U., & Llinás, R. (2005) · Thalamus & Related Systems · doi:10.1017/s1472928805000063 · Cited by 52
“This conception is based on fundamentals of neuronal electrophysiology (Llinas, 1988; Steriade and Llinas, 1988), thalamocortical anatomy (Steriade et al., 1987; Jones, 1998), intraoperative recordings with surgical outcomes (Jeanmonod et al.”
Method
Cerebellar and thalamic stimulation treatment for epilepsy
Krauss, G. L., & Koubeissi, M. Z. (2007) · Springer eBooks · doi:10.1007/978-3-211-33081-4_40 · Cited by 51
“superficial cortical layers [40].”
Diverse beta burst waveform motifs characterize movement-related cortical dynamics
Szul, M. J., Papadopoulos, S., Alavizadeh, S., Daligaut, S., Schwartz, D., Mattout, J., & Bonaiuto, J. J. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102490 · Cited by 51
Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders.
Hof, P., & Sherwood, C. (2005) · Anatomical Record Part A-discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20252 · Cited by 55
“…may also represent a pedomorphic feature because these calcium-binding proteins appear first during development and in rodent, carnivores, and primates and are preferentially distributed in phylogenetically older neural systems (Glezer et al., 1993, 1998; Jones, 1998; Hof et al., 1999).”
Background
Brain-wide single neuron reconstruction reveals morphological diversity in molecularly defined striatal, thalamic, cortical and claustral neuron types
Peng, H., Xie, P., Liu, L., Kuang, X., Wang, Y., Qu, L., Gong, H., Jiang, S., Li, A., Ruan, Z., et al. (2019) · doi:10.1101/675280 · Cited by 47
Thalamocortical mechanisms regulating the relationship between transient beta events and human tactile perception
Law, R. G., Pugliese, S., Shin, H., Sliva, D. D., Lee, S., Neymotin, S., Moore, C., & Jones, S. R. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhab221 · Cited by 41
“Simulating beta event generation and hypothesized recruitment of long-time scale supragranular inhibition We have previously shown that 50ms bursts of excitatory synaptic input arriving at supragranular layers (i.e. the apical tuft arborization of cortical pyramidal neurons) can explain the prominent negative deflecti…”
BackgroundInfluential
Central thalamic deep brain stimulation to support anterior forebrain mesocircuit function in the severely injured brain
Schiff, N. D. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1547-0 · Cited by 49
“dominant projection to superficial cortical layers and more limited infragranular projections (Jones 1998).”
Background
Organization of primate amygdalar–thalamic pathways for emotions
Timbie, C. M., García‐Cabezas, M. Á., Zikopoulos, B., & Barbas, H. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000639 · Cited by 48
Cortical Responses to Single Mechanoreceptive Afferent Microstimulation Revealed with fMRI
Trulsson, M., Francis, S., Kelly, E. F., Westling, G., Bowtell, R. W., & McGlone, F. P. (2001) · NeuroImage · doi:10.1006/nimg.2000.0723 · Cited by 49
Electrophysiological characterization of synaptic connections between layer VI cortical cells and neurons of the nucleus reticularis thalami in juvenile rats
Gentet, L. J., & Ulrich, D. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03168.x · Cited by 48
Forebrain control of breathing: Anatomy and potential functions
Schottelkotte, K. M., & Crone, S. A. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.1041887 · Cited by 51
A shifting role of thalamocortical connectivity in the emergence of cortical functional organization
Park, S., Haak, K. V., Oldham, S., Cho, H., Byeon, K., Park, B., Thomson, P., Chen, H., Gao, W., Xu, T., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01679-3 · Cited by 56
“Each subnucleus of the thalamus consists of a combination of excitatory neurons with distinct cell types that project differentially to the neocortex 7,100 .”
Variation of connectivity across exemplar sensory and associative thalamocortical loops in the mouse
Mukherjee, A., Bajwa, N., Lam, N. H., Porrero, C., Clascá, F., & Halassa, M. M. (2020) · eLife · doi:10.7554/elife.62554 · Cited by 49
“From this perspective, our findings and overall synthesis may be more in line with output-based classifications such as core vs. matrix (Jones, 1998; Jones, 2001).”
Result
Distinct anatomical connectivity patterns differentiate subdivisions of the nonlemniscal auditory thalamus in mice
Cai, D., Yue, Y., Su, X., Liu, M., Wang, Y., You, L., Xie, F., Deng, F., Chen, F., Luo, M., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhy115 · Cited by 45
Synchronization of Isolated Downstates (K-Complexes) May Be Caused by Cortically-Induced Disruption of Thalamic Spindling
Mak-McCully, R. A., Deiss, S. R., Rosen, B. Q., Jung, K.-Y., B, T. J. S. A., Bastuji, H., Rey, M. F., Cash, S. S., Bazhenov, M., & Halgren, E. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003855 · Cited by 47
“In a related fashion, our model also did not distinguish between matrix and core thalamocortical systems [64].”
Result
Molecular and spatial profiling of the paraventricular nucleus of the thalamus
Gao, C., Gohel, C., Leng, Y., Ma, J., Goldman, D. A., Levine, A. J., & Penzo, M. A. (2023) · eLife · doi:10.7554/elife.81818 · Cited by 49
“across unrestricted superficial cortical fields [69-71].”
T-type calcium channels in chronic pain: mouse models and specific blockers
François, A., Laffray, S., Pizzoccaro, A., Eschalier, A., & Bourinet, E. (2014) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1484-4 · Cited by 48
“these afferent tracts [57] and project to other cerebral areas of the pain matrix including the insula and the anterior cingulate”
Alarm or curse? The pain of neuroinflammation
Saab, C. Y., Waxman, S. G., & Hains, B. C. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.04.002 · Cited by 46
Clinical findings in sporadic Creutzfeldt-Jakob disease correlate with thalamic pathology
Tschampa, H. J. (2002) · Brain · doi:10.1093/brain/awf253 · Cited by 46
Unique combination of anatomy and physiology in cells of the rat paralaminar thalamic nuclei adjacent to the medial geniculate body
Smith, P. H., Bartlett, E. L., & Kowalkowski, A. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20913 · Cited by 45
Diencephalon
Puelles, L., Martı́nez-de-la-Torre, M., Ferrán, J. L., & WATSON, C. R. R. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10009-3 · Cited by 45
Thalamus
Mai, J. K., & Forutan, F. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374236-0.10019-7 · Cited by 45
Comparison of functional thalamic segmentation from seed-based analysis and ICA
Hale, J. R., Mayhew, S. D., Mullinger, K. J., Wilson, R. S., Arvanitis, T. N., Francis, S., & Bagshaw, A. P. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.04.027 · Cited by 45
“…agreement with anatomical segmentations of the thalamus from previous histological post-mortem work in humans (Morel et al., 1997) and primates (Jones, 1998), as well as non-invasive human structural (Behrens et al., 2003a; Johansen-Berg et al., 2005; Zhang et al., 2010) and functional…”
Background
A systematic topographical relationship between mouse lateral posterior thalamic neurons and their visual cortical projection targets
Juavinett, A., Kim, E. J., Collins, H. C., & Callaway, E. M. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24737 · Cited by 42
Spatiotemporal Expression of MANF in the Developing Rat Brain
Wang, H., Ke, Z., Alimov, A. P., Xu, M., Frank, J. A., Fang, S., & Luo, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090433 · Cited by 40
“Layer IV, the internal granular layer, contains different types of stellate and pyramidal neurons, and is the main target of thalamocortical afferents from thalamus type C neurons as well as intra-hemispheric cortico-cortical afferents [24].”
Pathways for emotions and memory II. Afferent input to the anterior thalamic nuclei from prefrontal, temporal, hypothalamic areas and the basal ganglia in the rhesus monkey
Xiao, D., & Barbas, H. (2002) · Thalamus & Related Systems · doi:10.1016/s1472-9288(02)00030-4 · Cited by 43
Interrogating the mouse thalamus to correct human neurodevelopmental disorders
Schmitt, L. I., & Halassa, M. M. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.183 · Cited by 41
Neocortex
Kirkcaldie, M. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10004-4 · Cited by 45
Crossmodal propagation of sensory-evoked and spontaneous activity in the rat neocortex
Takagaki, K., Zhang, C., Wu, J., & Lippert, M. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2007.11.069 · Cited by 39
Circuits through prefrontal cortex, basal ganglia, and ventral anterior nucleus map pathways beyond motor control
Xiaob, D., & Barbas, H. (2004) · Thalamus & Related Systems · doi:10.1016/j.tharel.2004.03.001 · Cited by 43
Diverse subthreshold cross‐modal sensory interactions in the thalamic reticular nucleus: implications for new pathways of cross‐modal attentional gating function
Kimura, A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12545 · Cited by 39
Locomotor Dysfunction and Pain: The Scylla and Charybdis of Fiber Sprouting After Spinal Cord Injury
Deumens, R., Joosten, E. A. J., Waxman, S. G., & Hains, B. C. (2008) · Molecular Neurobiology · doi:10.1007/s12035-008-8016-1 · Cited by 40
“cortical structures involved in the interpretation and conscious perception of pain [84].”
Cognitive consilience: Primate non-primary neuroanatomical circuits underlying cognition
Solari (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00065 · Cited by 41
Cortical and Thalamic Pathways for Multisensory and Sensorimotor Interplay
Cappe, C., Rouiller, E. M., & Barone, P. (2011) · Frontiers in neuroscience · doi:10.1201/b11092-4 · Cited by 48
Relay and higher-order thalamic nuclei show an intertwined functional association with cortical-networks
Kumar, V., Beckmann, C. F., Scheffler, K., & Grodd, W. (2022) · Communications Biology · doi:10.1038/s42003-022-04126-w · Cited by 38
Pathway mechanism for excitatory and inhibitory control in working memory
Barbas, H., Wang, J., Joyce, M. K. P., & García‐Cabezas, M. Á. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00936.2017 · Cited by 38
“Neurons that are positive for PV, CB, or CR in the thalamus are not inhibitory, but represent projection classes directed to the cortex (Jones 1998; Rausell and Jones 1991a, 1991b; Rausell et al. 1992; Timbie and Barbas 2014).”
Mapping Functional Connectivity from the Dorsal Cortex to the Thalamus
Huo, Y., Chen, H., & Guo, Z. V. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.038 · Cited by 38
Effects of high-frequency skin stimulation on SI cortex: Mechanisms and functional implications
Tommerdahl, M., Favorov, O. V., & Whitsel, B. L. (2005) · Somatosensory & Motor Research · doi:10.1080/08990220500084461 · Cited by 38
Growth and refinement of excitatory synapses in the human auditory cortex
Pundir, A. S., Singh, U. A., Ahuja, N., Makhija, S., Dikshit, P. C., Radotra, B. D., Kumar, P., Shankar, S. K., Mahadevan, A., Roy, T. S., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1124-6 · Cited by 37
The Central Lateral Thalamotomy for Neuropathic Pain
Jeanmonod, D., & Morel, A. (2009) · Springer eBooks · doi:10.1007/978-3-540-69960-6_123 · Cited by 37

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)
DOI: 10.1016/s0306-4522(97)00581-2
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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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