Viewpoint: the core and matrix of thalamic organization

“Anatomical studies in monkeys outline three main routes which nonauditory inputs may use to access auditory cortex: (1) feedforward projections from ‘‘nonspecific’’ thalamic afferents (Hackett et al., 1998b; Jones, 1998), (2) direct lateral projections from low-level nonauditory cortices (Falchier et al.”

“This is particularly true for the thalamus (Jones 1998) and the brainstem (Parvizi &”

“…elicits a sensation of pain, it is reasonable to assume that the elicited brain responses are at least partially pain specific (Talbot et al. 1991; Jones 1998a; Ingvar 1999; Ingvar and Hsieg 1999; Ploghaus et al. 1999; Avenanti et al. 2005; Brooks and Tracey 2005; Stern et al. 2006; Tracey and…”

“Jones [41,42] refers to the specific and nonspecific systems as the ‘core’ and ‘matrix’ components of the thalamocortical projection.”

“They establish and maintain synchrony across ensembles of cortical neurons that is observed over widespread areas of cortex (Herkenham, 1986; Castro-Alamancos, 1997; Jones, 1998a, 2001).”

“Jones (1998) has suggested that diffuse projecting thalamic neurons are not con®ned to the intralaminar nuclei and are present throughout the thalamus.”

“In addition, nonspecific thalamic nuclei, which may act as classic modulatory inputs in auditory cortex, project diffusely and nonspecifically to the superficial cortical layers of several cortical fields (Jones, 1998).”

“…in the attention-related modulation of evoked type and modulatory neuronal activity supports distinct sets of driving and modulatory type inputs that generate/orchestrate them, as suggested earlier (Sherman and Guillery, 1998; Jones, 1998a, 1998b; Lakatos et al., 2009; Viaene et al., 2011).”

“…pulvino-cortical projections, because projections to the middle layers (4 and 3) are found to arise only from parvalbumin-positive projection neurons, whereas the more diffuse projections to superficial layers, including layer 1, are made by calbindin-positive projection neurons (Jones 1998, 2001).”

“…useful to study the development of specific systems as well as their evolution, as these calcium-binding proteins exhibit preferential distribution within functionally distinct pathways (Rausell et al., 1992; Glezer et al., 1993, 1999; Hashikawa et al., 1995; Molinari et al., 1995; Jones, 1998).”

“Nonspecific inputs, that is those that do not convey a precise, focal representation of the receptor surface, are transmitted by the calbindin expressing neurons of the socalled ‘‘thalamic matrix’’ and project more widely to the supragranular layers of cortex (Jones, 1998a, 1998b).”

“To narrow down the list of possible long-range pathways affected in autism, we labeled axons with the calcium-binding proteins calbindin or parvalbumin, which are expressed by distinct classes of excitatory thalamic neurons that project to the cortex (Jones, 1998, 2007; Zikopoulos and Barbas, 2007).”

“This organization suggests important functional roles for corticofugal pathways, possibly implementing additional and indirect corticocortical routes through the thalamus (Jones, 1998; Sherman, 2005, 2012).”

“However, the calbindin cells spread throughout the nucleus and are continuous with a larger population of calbindin cells in the adjoining inferior pulvinar nucleus (Jones 1998).”

“The cerebellar cortex also lacks the ‘crowning mystery’ – layer I, which is one important target for longrange feedback connections and nonspecific thalamic inputs [33,35].”

“, limbic (30)] and underrepresented [dorsal attention and visual in striatum (74); visual in cerebellum (32)] networks were excluded (see SI Appendix for further details).”

“However, individual midline and intralaminar nuclei receive distinct sets of inputs and project to restricted areas of the neocortex (Groenewegen and Berendse, 1994; Jones, 1998; Van der Werf et al., 2002).”

“, the suprageniculate or the limitans nucleus), the koniocellular matrix neurons and forebrain structures project diffusely to the sensory cortices (Morel and Kaas 1992; Pandya et al. 1994; Jones 1998; Zaborszky and Duque 2000; Zaborszky 2002; Budinger et al. 2006; de la Mothe et al. 2006).”

“, 2007) and the thalamus is increasingly regarded as a potentially major player in multisensory phenomena (Jones, 1998; Schroeder et al., 2003; Fu et al., 2004; Ghazanfar and Schroeder, 2006), we did not observe any BOLD effects in the thalaFigure 3.”

“distinct projection patterns are often denoted as ‘‘matrix’’ or ‘‘core,’’ respectively (Jones, 1998).”

“the LGN, play these different roles, the calbindin immunoreactive cells (in primate) contributing to secondary or association thalamus, or matrix, and the parvalbumin immuno-reactive cells contributing to the primary sensory, or core regions (Jones, 1998).”

“…thalamus (Jones, 1998, 2001; Clascá et al., 2012), where core cells are abundant in the ventral portion of MGB (MGv) that receives lemniscal inputs, whereas matrix cells, targeted by non-lemniscal fibers, prevail in the dorsal and caudo-medial MGB (MGd/MGm) (Jones, 1998; Clascá et al., 2012).”

“a 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 999‐1014 calbindin-negative relay cells (which are positive in certain species for parvalbumin) prevail in first-order nuclei ( Jones, 1998 ).”

“, 1986), and secondary ascending sensory system (Herkenham, 1979; Casagrande, 1994; Jones, 1998).”

“In contrast, PV positive neurons are prevalent in topographically specific sensory thalamic nuclei that project selectively to the middle layers of the cortex (Jones, 1998).”

“c-layer I is populated by only a few scattered non-pyramidal neurons (Cajal-Retzius and spiny stellate cells), but mainly contains the terminal ramifications of apical dendrites of pyramidal neurons of deeper layers, and horizontally oriented axons from M-type thalamic neurons (Cajal-Retzius stripe in myeloarchitectur…”

“Specifically, cortical inputs are integrated within the basal ganglia and thalamus before being projected diffusely to multiple cortical networks (Alexander et al., 1986; Averbeck et al., 2014; Draganski et al., 2008; Jarbo and Verstynen, 2015; Jones, 1998; Metzger et al., 2013).”

“Dorsal horn nociceptive neurons project rostrally to thirdorder neurons in the ventral posterolateral (VPL) nucleus of the thalamus, which is involved in sensory-discriminative aspects of pain processing (Jones 1998).”

“…the cortical layer I, it is likely that some of these projections providing multimodal information to the cortex originate from the so-called ‘‘matrix’’ calbindin-immunoreactive neurons distributed in all thalamic nuclei and projecting diffusely and relatively widely to the cortex (Jones 1998).”

“…Rausell and Jones (1991a, b, 1992) described small calbindin-positive neurons within VPM and VPL that they considered to constitute a 'matrix' in these and other dorsal thalamic nuclei (Jones, 1998), and they reported that these neurons receive ascending spino-and trigeminothalamic projections.”

“…calbindin and parvalbumin; the former (calbindinpositive ) form a matrix with terminals in superficial cortical layers, the latter (parvalbumin-positive) are localized to specific thalamic nuclei and form a core that projects to middle cortical layers (for review, Jones, 1998, 2001, 2002, 2009).”

“At least three broad TC cell types (Herkenham, 1986; Castro-Alamancos & Connors, 1997; Jones, 1998, 2007; Huang & Winer, 2000) can be identified based on such axonal differences (Table 1): intralaminar-type (IL-type), matrix-type (M-type) and coretype (C-type) neurons.”

“VAL instead projects in a more focal manner to middle layers (‘core’) (Jones, 1998; Kuramoto et al., 2015).”

“…dorsal horn nociceptive neurons pro- ject rostrally within the spinothalamic tract, and synapse on third-order neurons of the ventroposterior lateral (VPL) nucleus of the thalamus (Jones, 1998; Willis and Coggeshall, 2004), which is involved in sensory discriminative aspects of pain processing.”

“Such cells may parallel in their projections and actions the Calb glutamatergic neurons of the thalamus (Frassoni et al., 1997), which provide a widespread projection to the superficial layers of the cerebral cortex (Rausell and Jones, 1991; Jones, 1998).”

“…et al., 2000; Steinmetz et al., 2000; Eimer and Forster, 2003; de Lafuente and Romo, 2006; Moore et al., 2007) and in FC during tactile detection (de Lafuente and Romo, 2005, 2006; Palva et al., 2005), and implicated in a class of thalamic neurons that project directly to SGR (Jones, 1998, 2001).”

“Strangely, the LGN projections to the extrastriate cortex terminate neither in layer 4, which is characteristic of feedforward thalamic projections, nor in the supragranular layers, which is characteristic of modulatory thalamic connections ( Jones 1998).”

“Most inputs to layer 1 originate from the higher-order cortical areas (Zeki & Shipp, 1988; Johnson & Burkhalter, 1997; Cauller et al. 1998), cholinergic and monoaminergic systems (De Lima & Singer, 1986; Lysakowski et al. 1986), and secondary sensory ascending system (Herkenham, 1980; Jones, 1998).”

“…is based on an understanding of the intrinsic oscillatory properties of thalamic neurons (Jahnsen and Llinas, 1984; Llinas, 1988; Steriade and Llinas, 1988; Jeanmonod et al., 1996) thalamocortical anatomy (Jones, 1998), and biochemical influences on the thalamocortical circuit (Behrendt, 2006).”

“the former have been referred to as “core,” and the latter, as “matrix” (72).”

“In addition to the frequently described “core” projections from the sensory nuclei of the thalamus to layer IV of sensory cortices, the thalamus is known to have less-specific, more-diffuse cortical projections (Jones, 1998).”

“…terminate as large and round clusters of terminals in sensory thalamic nuclei and innervate the proximal dendrites of thalamic neurons (Jones and Hendry, 1989; Guillery, 1995; Rockland, 1996; Jones, 1998a; Jones, 1998b; Rockland et al., 1999; Rouiller and Welker, 2000; Guillery and Sherman, 2002).”

“Upon this matrix is superimposed a core of parvalbumin-expressing cells, enclosed by the classically defined sensory and motor relay nuclei, that project to the middle layers of the cortex in strict topographic order (Jones, 1998, 2007).”

“It has been proposed that primate and carnivore thalamic projection neurons are classified into core-type and matrix-type neurons (for a review, see Jones, 1998).”

“…that neocortical layer 1 is not merely a site for feedback connections but is also an explicit target of first and higher order thalamic nuclei (Jones, 1998; Rubio-Garrido et al., 2009) as well as of feedforward projections between higher (non-primary) areas of a cortical hierarchy (Coogan and…”

“…of matrix-type TC projections, ramify densely in layer 1 (Herkenham, 1979; Arbuthnott et al., 1990; Kuramoto et al., 2015), whereas VL projections, which accord more with core-type TC projections, ramify mainly in layers 4 and 5B (Jones, 1998; Clascá et al., 2012; Yamawaki et al., 2014).”

“…cholinergic inputs (Sherman and Guillery, 1998, 2002; Rouiller and Welker, 2000; Guillery and Sherman, 2002) which in turn dynamically alter information received by cortical regions (Jones, 1998; Sherman and Guillery, 1998, 2002; Rouiller and Welker, 2000; Haber and McFarland, 2001; Jones, 2001).”

“…contain small boutons that predominantly interact with metabotropic glutamate receptors to modify neuronal activity (Casagrande, Guillery, & Sherman, 2005; Guillery, 1995; Guillery & Sherman, 2002; Jones, 1998a, 1998b; Reichova & Sherman, 2004; Rouiller & Welker, 2000; Sherman & Guillery, 1998).”

“’s study included cortical layer I, it is likely hat some of these projections, providing multimodal information o the cortex, originated from the so-called ‘matrix’, or nonpecific neurons distributed in all thalamic nuclei, which project iffusely to the cerebral cortex (Jones, 1998).”

“emotional aspects of pain, including the insula and the AAC[56].”

“In addition, the primary and topographically precise ‘core’ projection of each thalamic nucleus to the middle layers of its cortical target region is now known to be accompanied by a more diffuse and widespread ‘matrix’ projection from the same nucleus, targeted to the upper layers of the same region [33].”

“Historically, the thalamic relay neurons have been divided in two fundamentally different sets: parvalbumin-positive ‘‘core’’ neurons, which form topographically organized projections to middle layers of cerebral cortical patches, and calbindin-positive ‘‘matrix’’ neurons, which send more diffuse projections to the co…”

“Dorsal horn neurons project rostrally within the spinothalamic tract to third-order neurons of the ventroposterior lateral (VPL) nucleus of the thalamus ( Jones, 1998 ).”

“As reviewed earlier (Jones 1998), there are two thalamic sensory systems: a core system that projects topographically (or tonotopically) organized sensory information to welldefined primary sensory cortical areas and a matrix system, composed of koniocellular neurons that project less specific…”

“, 2005b), and that anesthetics selectively suppress “matrix” thalamic nuclei, which provide largely modulatory TC input, compared to “core” thalamic nuclei, which provide largely driving TC input (Jones, 1998; Liu et al., 2013; Saalmann, 2014).”