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Functioning of Circuits Connecting Thalamus and Cortex

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ABSTRACT

Glutamatergic pathways in thalamus and cortex are divided into two distinct classes: driver, which carries the main information between cells, and modulator, which modifies how driver inputs function. Identifying driver inputs helps to reveal functional computational circuits, and one set of such circuits identified by this approach are cortico‐thalamo‐cortical (or transthalamic corticocortical) circuits. This, in turn, leads to the conclusion that there are two types of thalamic relay: first order nuclei (such as the lateral geniculate nucleus) that relay driver input from a subcortical source (i.e., retina), and higher order nuclei (such as the pulvinar) which are involved in these transthalamic pathways by relaying driver input from layer 5 of one cortical area to another. This thalamic division is also seen in other sensory pathways and beyond these so that most of thalamus by volume consists of higher‐order relays. Many, and perhaps all, direct driver connections between cortical areas are paralleled by an indirect cortico‐thalamo‐cortical (transthalamic) driver route involving higher order thalamic relays. Such thalamic relays represent a heretofore unappreciated role in cortical functioning, and this assessment challenges and extends conventional views regarding both the role of thalamus and mechanisms of corticocortical communication. Finally, many and perhaps the vast majority of driver inputs relayed through thalamus arrive via branching axons, with extrathalamic targets often being subcortical motor centers. This raises the possibility that inputs relayed by thalamus to cortex also serve as efference copies, and this may represent an important feature of information relayed up the cortical hierarchy via transthalamic circuits. © 2017 American Physiological Society. Compr Physiol 7:713‐739, 2017.

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Figure 1. Figure 1. Schematic three‐dimensional view of right thalamus with many of its major nuclei. A cut is placed in the posterior part to reveal a representative cross‐section. To prevent obscuring the dorsal thalamus, only the rostral tip of the TRN is shown. Abbreviations: A, anterior nucleus; CM, centromedian nucleus; IL, intralaminar nuclei; IML, internal medullary lamina; LD, lateral dorsal nucleus; LP, lateral posterior nucleus; LGN, lateral geniculate nucleus; MGN, medial geniculate nucleus; MD, mediodorsal nucleus; MI, midline nuclei; P, pulvinar; PO, posterior nucleus; TRN, thalamic reticular nucleus; VA, ventral anterior nucleus; VPl, ventral posterolateral nucleus; VPm, ventral posteromedial nucleus. See Jones () for details of connectivity of these nuclei. Redrawn, with permission, from ().
Figure 2. Figure 2. Reconstruction of representative thalamic cells types from the lateral geniculate nucleus of the cat based on intracellular dye filling of individual, physiologically identified neurons. (A) Relay X and Y cell. (B) Interneuron. The inset shows the presynaptic bouton terminals emanating from dendrites. (C) Cell of the thalamic reticular nucleus. The larger scale applies to the inset for the interneuron. A and B, with permission, from (); and C, with permission, from ().
Figure 3. Figure 3. (A) Schematic and simplified view of thalamic circuitry. The various inputs to the different thalamic cell types are displayed, and the excitatory or inhibitory postsynaptic effect. (B and C) Schematic view of different possible circuits involving layer 6 corticothalamic input to reticular cells, interneurons, and relay cells. See text for details. Abbreviations: 5‐HT, serotonin; ACh, acetylcholine; BRF, brainstem reticular formation; GABA, γ‐aminobutyric acid; Glu, glutamate; NA, noradrenaline; TRN, thalamic reticular nucleus.
Figure 4. Figure 4. Schematic views of features of connectivity in the A layers of the cat's lateral geniculate nucleus. (A) Synaptic inputs in and near a glomerulus. Shown are the various synaptic contacts (arrows), whether they are inhibitory or excitatory, and the related postsynaptic receptors. The conventional triad includes the lower interneuronal dendritic terminal and involves three synapses (from the retinal terminal to the dendritic terminal, from the retinal terminal to an appendage of the X cell dendrite, and from the dendritic terminal to the same appendage). Another type of triad includes the upper interneuronal dendritic terminal and also involves three synapses: a branched (cholinergic) brainstem axon produces one synaptic terminal onto an X cell relay dendrite and another onto the dendritic terminal, and a third synapse is formed from the dendritic terminal onto the same relay cell dendrite. For simplicity, the NMDA receptor on the relay cell postsynaptic to the retinal input has been left off. (B) Synaptic inputs onto an X and a Y cell. For simplicity, only one, unbranched dendrite is shown. Synaptic types are shown in relative numbers. Abbreviations: ACh, acetylcholine; AMPAR, (R,S)‐α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid receptor; GABA, γ‐aminobutyric acid; GABAAR, type A receptor for GABA; Glu, glutamate; M1R and M2R, two types of muscarinic receptor; mGluR5, type 5 metabotropic glutamate receptor; NicR, nicotinic receptor. Redrawn, with permission, from ().
Figure 5. Figure 5. Overview of circuitry of LGN. (A and B) Detailed circuitry for X and Y relay cells of the LGN of the cat. The inhibitory inputs from axons of interneurons to relay cells is of the opposite center/surround type. For the center/surround receptive field icons, plusses refer to on areas, and minuses, to off areas. Redrawn, with permission, from (). Abbreviations: I, interneuron; LGN, lateral geniculate nucleus; R, LGN relay cell; TRN, thalamic reticular nucleus.
Figure 6. Figure 6. Burst and tonic firing based on IT properties. Adapted, with permission, from (). (A) IT becomes inactivated following ≥∼100 ms of membrane depolarization relative to about −60 to 65 mV, and the inactivation is removed (or, IT is deinactivated) by an equivalent time of relative hyperpolarization. (A) Tonic firing results when IT is inactivated. (B) Burst firing results when IT is deinactivated. (C) Input–output relationship for a single cell. The abscissa is the amplitude of the depolarizing current pulse and the ordinate is the firing frequency of the cell. The firing frequency was determined by the first six action potentials of the response, burst or tonic, because this cell normally exhibited six action potentials per burst in this experiment. The initial holding potentials are shown: −47 and −59 mV reflects tonic mode (blue points and curves), whereas −77 and −83 mV reflects burst mode (red points and curves).
Figure 7. Figure 7. Different receptive field properties involved in responses of geniculate relay cells. Those of the retinal input display the classic center/surround structure, and these are monocularly represented. Those of the layer 6 cortical input have more complex features, including orientation and direction selectivity, and these are binocularly represented. Those of the geniculate cell have features much like those of its retinal input and unlike its cortical input.
Figure 8. Figure 8. Drivers and modulators. (A) Modulators (dashed green inputs) shown contacting more peripheral dendrites than do drivers (solid green input). Also, drivers activate only ionotropic glutamate receptors, whereas modulators also activate metabotropic glutamate receptors. (B) Effects of repetitive stimulation on EPSP amplitude: for modulators, this produces paired pulse facilitation (increasing EPSP amplitudes during the stimulus train), whereas for drivers, this produces paired pulse depression (decreasing EPSP amplitudes during the stimulus train). Also, increasing stimulus intensity for modulators (shown as different colors) increases EPSPs more than is the case for drivers; this indicates more convergence of modulator inputs compared to driver inputs. (C) Light microscopic tracings of a driver afferent (a retinogeniculate axon from the cat) and a modulator afferent (a corticogeniculate axon from layer 6 of the cat). Redrawn, with permission, from (). (D) Three‐dimensional scatterplot for inputs classified as driver or modulator to cells of thalamus and cortex; data from in vitro slice experiments in mice from the author's laboratory. The three parameters are: (1) the amplitude of the first EPSP elicited in a train at a stimulus level just above threshold; (2) a measure of paired‐pulse effects (the amplitude of the second EPSP divided by the first) for stimulus trains of 10 to 20 Hz; and (3) a measure of the response to synaptic activation of metabotropic glutamate receptors, taken as the maximum voltage deflection (i.e., depolarization or hyperpolarization) during the 300 ms postsynaptic response period to tetanic stimulation in the presence of AMPA and NMDA blockers. Pathways tested here include various inputs to thalamus from cortex and subcortical sources, various thalamocortical pathways, and various intracortical pathways. Adapted, with permission, from ().
Figure 9. Figure 9. Schematic summary of synaptic effects of layer 6 corticothalamic cells on thalamocortical transmission. Note that these cells have bifurcating axons that innervate both layer 4 cells postsynaptic to thalamic input as well as thalamic circuitry. Four distinct effects have been documented, each of which serves to reduce the gain of thalamocortical transmission. See text for details.
Figure 10. Figure 10. Schematic diagrams showing organizational features of first and higher order thalamic nuclei. A first‐order nucleus (left) represents the first relay of a particular type of subcortical information to a first‐order or primary cortical area. A higher‐order nucleus (center and right) relays information from layer 5 of one cortical area up the hierarchy to another cortical area. This relay can be from a primary area to a higher one (center) or between two higher‐order cortical areas (right). The important difference between first‐ and higher‐order nuclei is the driver input, which is subcortical for a first‐order relay and from layer 5 of cortex for a higher‐order relay. Note that all thalamic nuclei receive an input from layer 6 of cortex, which is mostly organized in a reciprocal feedback manner, but higher‐order nuclei in addition receive a layer 5 input from cortex, which is feedforward. Note that the driver inputs, both subcortical and from layer 5, are typically from branching axons, with some extrathalamic targets being subcortical motor centers, and the significance this is elaborated in the text. Abbreviations: BRF, brainstem reticular formation; FO, first order; HO, higher order; TRN, thalamic reticular nucleus. Redrawn, with permission, from ().
Figure 11. Figure 11. Two views of tectothalamic inputs in auditory pathways. Shown are projections from the core region of the inferior colliculus (ICc) to the ventral part of the medial geniculate nucleus (MGNv) and from the shell region of the inferior colliculus (ICs) to the dorsal part of the medial geniculate nucleus (MGNd). (A) View of parallel processing. Two information streams are shown, one from ICc through MGNv to primary auditory cortex (A1) and the other from ICs through MGNd to secondary auditory cortex (A2). (B) View incorporating identification of drivers and modulators. The stream from ICc through MGNv involves driver paths and thus represents an information stream. However, the input from ICs to MGNd is a modulator, whereas the driver input to MGNd arises from layer 5 of cortex. Thus, in this view, the projection from ICs to MGNd modulates this transthalamic circuit.
Figure 12. Figure 12. Two views of the relationship between the basal ganglia and cortex. (A) Textbook view. This depicts a simple information loop, the information flowing from thalamus to cortex to basal ganglia to thalamus, etc. Adapted, with permission, from (). (B) Different view incorporating the idea that information is carried by glutamatergic driver pathways. Since the basal ganglia outputs are strictly GABAergic, this input to thalamus serves not as an information route but rather modulates a transthalamic pathway through the higher‐order portion of the motor thalamus. When active, the basal ganglia input would shut down the higher‐order thalamic relays, providing a gating mechanism. (C) One example of this is that the basal ganglia input to thalamus can determine which combinations of transthalamic pathways are active at any given time; dashed thalamocortical pathways indicate that these are nonactive due to basal ganglia inhibition. (D) A related example is that the basal ganglia can determine which cortical areas are actively connected by both direct and transthalamic pathways, and not just the former. See text for details.
Figure 13. Figure 13. Branching driver inputs to representative first order thalamic relays. (A) Example from retinogeniculate axon of cat; redrawn, with permission, from (). (B) Example of cerebellar inputs to the ventral anterior and ventral lateral nuclei (VA/VL); redrawn, with permission, from (), and thanks to Javier deFelipe for providing this image. (C) Example of mammillary inputs to the anterior dorsal nucleus (AD); redrawn, with permission, from (). Red arrows in B and C indicate branch points.
Figure 14. Figure 14. Example from layer 5 pyramidal tract cell of rat motor cortex; redrawn, with permission, from (); tracing of reconstruction generously supplied by H. Kita. Branches innervating thalamus are indicated by the dashed blue circle, and brainstem motor regions are indicated by red arrows. Abbreviations: cp, cerebral peduncle; DpMe, deep mesencephalic nuclei; Gi, gigantocellular reticular nucleus; GPe, Globus pallidus external segment; ic, internal capsule; IO, inferior olive; Pn, pontine nucleus; PnO, pontine reticular nucleus, oral part; py, medullary pyramid; pyd, pyramidal decussation; Rt, thalamic reticular nucleus; SC, superior colliculus; SN, substantia nigra; Str, striatum; VL, ventrolateral thalamic nucleus; VM, ventromedial thalamic nucleus.
Figure 15. Figure 15. Branching axons. (A) Cajal illustration () of primary axons entering the spinal cord and branching to innervate the spinal gray matter and brain areas. The red arrows indicate branch points. Thanks to Javier deFelipe for providing this image. (B) Schematic interpretation of A.
Figure 16. Figure 16. Comparison of conventional view (A) with the alternative view proposed here (B). The question marks in A indicate higher order thalamic relays, for which no specific function is suggested in this scheme. Further details in text. Abbreviations: FO, first order; HO, higher order.


Figure 1. Schematic three‐dimensional view of right thalamus with many of its major nuclei. A cut is placed in the posterior part to reveal a representative cross‐section. To prevent obscuring the dorsal thalamus, only the rostral tip of the TRN is shown. Abbreviations: A, anterior nucleus; CM, centromedian nucleus; IL, intralaminar nuclei; IML, internal medullary lamina; LD, lateral dorsal nucleus; LP, lateral posterior nucleus; LGN, lateral geniculate nucleus; MGN, medial geniculate nucleus; MD, mediodorsal nucleus; MI, midline nuclei; P, pulvinar; PO, posterior nucleus; TRN, thalamic reticular nucleus; VA, ventral anterior nucleus; VPl, ventral posterolateral nucleus; VPm, ventral posteromedial nucleus. See Jones () for details of connectivity of these nuclei. Redrawn, with permission, from ().


Figure 2. Reconstruction of representative thalamic cells types from the lateral geniculate nucleus of the cat based on intracellular dye filling of individual, physiologically identified neurons. (A) Relay X and Y cell. (B) Interneuron. The inset shows the presynaptic bouton terminals emanating from dendrites. (C) Cell of the thalamic reticular nucleus. The larger scale applies to the inset for the interneuron. A and B, with permission, from (); and C, with permission, from ().


Figure 3. (A) Schematic and simplified view of thalamic circuitry. The various inputs to the different thalamic cell types are displayed, and the excitatory or inhibitory postsynaptic effect. (B and C) Schematic view of different possible circuits involving layer 6 corticothalamic input to reticular cells, interneurons, and relay cells. See text for details. Abbreviations: 5‐HT, serotonin; ACh, acetylcholine; BRF, brainstem reticular formation; GABA, γ‐aminobutyric acid; Glu, glutamate; NA, noradrenaline; TRN, thalamic reticular nucleus.


Figure 4. Schematic views of features of connectivity in the A layers of the cat's lateral geniculate nucleus. (A) Synaptic inputs in and near a glomerulus. Shown are the various synaptic contacts (arrows), whether they are inhibitory or excitatory, and the related postsynaptic receptors. The conventional triad includes the lower interneuronal dendritic terminal and involves three synapses (from the retinal terminal to the dendritic terminal, from the retinal terminal to an appendage of the X cell dendrite, and from the dendritic terminal to the same appendage). Another type of triad includes the upper interneuronal dendritic terminal and also involves three synapses: a branched (cholinergic) brainstem axon produces one synaptic terminal onto an X cell relay dendrite and another onto the dendritic terminal, and a third synapse is formed from the dendritic terminal onto the same relay cell dendrite. For simplicity, the NMDA receptor on the relay cell postsynaptic to the retinal input has been left off. (B) Synaptic inputs onto an X and a Y cell. For simplicity, only one, unbranched dendrite is shown. Synaptic types are shown in relative numbers. Abbreviations: ACh, acetylcholine; AMPAR, (R,S)‐α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid receptor; GABA, γ‐aminobutyric acid; GABAAR, type A receptor for GABA; Glu, glutamate; M1R and M2R, two types of muscarinic receptor; mGluR5, type 5 metabotropic glutamate receptor; NicR, nicotinic receptor. Redrawn, with permission, from ().


Figure 5. Overview of circuitry of LGN. (A and B) Detailed circuitry for X and Y relay cells of the LGN of the cat. The inhibitory inputs from axons of interneurons to relay cells is of the opposite center/surround type. For the center/surround receptive field icons, plusses refer to on areas, and minuses, to off areas. Redrawn, with permission, from (). Abbreviations: I, interneuron; LGN, lateral geniculate nucleus; R, LGN relay cell; TRN, thalamic reticular nucleus.


Figure 6. Burst and tonic firing based on IT properties. Adapted, with permission, from (). (A) IT becomes inactivated following ≥∼100 ms of membrane depolarization relative to about −60 to 65 mV, and the inactivation is removed (or, IT is deinactivated) by an equivalent time of relative hyperpolarization. (A) Tonic firing results when IT is inactivated. (B) Burst firing results when IT is deinactivated. (C) Input–output relationship for a single cell. The abscissa is the amplitude of the depolarizing current pulse and the ordinate is the firing frequency of the cell. The firing frequency was determined by the first six action potentials of the response, burst or tonic, because this cell normally exhibited six action potentials per burst in this experiment. The initial holding potentials are shown: −47 and −59 mV reflects tonic mode (blue points and curves), whereas −77 and −83 mV reflects burst mode (red points and curves).


Figure 7. Different receptive field properties involved in responses of geniculate relay cells. Those of the retinal input display the classic center/surround structure, and these are monocularly represented. Those of the layer 6 cortical input have more complex features, including orientation and direction selectivity, and these are binocularly represented. Those of the geniculate cell have features much like those of its retinal input and unlike its cortical input.


Figure 8. Drivers and modulators. (A) Modulators (dashed green inputs) shown contacting more peripheral dendrites than do drivers (solid green input). Also, drivers activate only ionotropic glutamate receptors, whereas modulators also activate metabotropic glutamate receptors. (B) Effects of repetitive stimulation on EPSP amplitude: for modulators, this produces paired pulse facilitation (increasing EPSP amplitudes during the stimulus train), whereas for drivers, this produces paired pulse depression (decreasing EPSP amplitudes during the stimulus train). Also, increasing stimulus intensity for modulators (shown as different colors) increases EPSPs more than is the case for drivers; this indicates more convergence of modulator inputs compared to driver inputs. (C) Light microscopic tracings of a driver afferent (a retinogeniculate axon from the cat) and a modulator afferent (a corticogeniculate axon from layer 6 of the cat). Redrawn, with permission, from (). (D) Three‐dimensional scatterplot for inputs classified as driver or modulator to cells of thalamus and cortex; data from in vitro slice experiments in mice from the author's laboratory. The three parameters are: (1) the amplitude of the first EPSP elicited in a train at a stimulus level just above threshold; (2) a measure of paired‐pulse effects (the amplitude of the second EPSP divided by the first) for stimulus trains of 10 to 20 Hz; and (3) a measure of the response to synaptic activation of metabotropic glutamate receptors, taken as the maximum voltage deflection (i.e., depolarization or hyperpolarization) during the 300 ms postsynaptic response period to tetanic stimulation in the presence of AMPA and NMDA blockers. Pathways tested here include various inputs to thalamus from cortex and subcortical sources, various thalamocortical pathways, and various intracortical pathways. Adapted, with permission, from ().


Figure 9. Schematic summary of synaptic effects of layer 6 corticothalamic cells on thalamocortical transmission. Note that these cells have bifurcating axons that innervate both layer 4 cells postsynaptic to thalamic input as well as thalamic circuitry. Four distinct effects have been documented, each of which serves to reduce the gain of thalamocortical transmission. See text for details.


Figure 10. Schematic diagrams showing organizational features of first and higher order thalamic nuclei. A first‐order nucleus (left) represents the first relay of a particular type of subcortical information to a first‐order or primary cortical area. A higher‐order nucleus (center and right) relays information from layer 5 of one cortical area up the hierarchy to another cortical area. This relay can be from a primary area to a higher one (center) or between two higher‐order cortical areas (right). The important difference between first‐ and higher‐order nuclei is the driver input, which is subcortical for a first‐order relay and from layer 5 of cortex for a higher‐order relay. Note that all thalamic nuclei receive an input from layer 6 of cortex, which is mostly organized in a reciprocal feedback manner, but higher‐order nuclei in addition receive a layer 5 input from cortex, which is feedforward. Note that the driver inputs, both subcortical and from layer 5, are typically from branching axons, with some extrathalamic targets being subcortical motor centers, and the significance this is elaborated in the text. Abbreviations: BRF, brainstem reticular formation; FO, first order; HO, higher order; TRN, thalamic reticular nucleus. Redrawn, with permission, from ().


Figure 11. Two views of tectothalamic inputs in auditory pathways. Shown are projections from the core region of the inferior colliculus (ICc) to the ventral part of the medial geniculate nucleus (MGNv) and from the shell region of the inferior colliculus (ICs) to the dorsal part of the medial geniculate nucleus (MGNd). (A) View of parallel processing. Two information streams are shown, one from ICc through MGNv to primary auditory cortex (A1) and the other from ICs through MGNd to secondary auditory cortex (A2). (B) View incorporating identification of drivers and modulators. The stream from ICc through MGNv involves driver paths and thus represents an information stream. However, the input from ICs to MGNd is a modulator, whereas the driver input to MGNd arises from layer 5 of cortex. Thus, in this view, the projection from ICs to MGNd modulates this transthalamic circuit.


Figure 12. Two views of the relationship between the basal ganglia and cortex. (A) Textbook view. This depicts a simple information loop, the information flowing from thalamus to cortex to basal ganglia to thalamus, etc. Adapted, with permission, from (). (B) Different view incorporating the idea that information is carried by glutamatergic driver pathways. Since the basal ganglia outputs are strictly GABAergic, this input to thalamus serves not as an information route but rather modulates a transthalamic pathway through the higher‐order portion of the motor thalamus. When active, the basal ganglia input would shut down the higher‐order thalamic relays, providing a gating mechanism. (C) One example of this is that the basal ganglia input to thalamus can determine which combinations of transthalamic pathways are active at any given time; dashed thalamocortical pathways indicate that these are nonactive due to basal ganglia inhibition. (D) A related example is that the basal ganglia can determine which cortical areas are actively connected by both direct and transthalamic pathways, and not just the former. See text for details.


Figure 13. Branching driver inputs to representative first order thalamic relays. (A) Example from retinogeniculate axon of cat; redrawn, with permission, from (). (B) Example of cerebellar inputs to the ventral anterior and ventral lateral nuclei (VA/VL); redrawn, with permission, from (), and thanks to Javier deFelipe for providing this image. (C) Example of mammillary inputs to the anterior dorsal nucleus (AD); redrawn, with permission, from (). Red arrows in B and C indicate branch points.


Figure 14. Example from layer 5 pyramidal tract cell of rat motor cortex; redrawn, with permission, from (); tracing of reconstruction generously supplied by H. Kita. Branches innervating thalamus are indicated by the dashed blue circle, and brainstem motor regions are indicated by red arrows. Abbreviations: cp, cerebral peduncle; DpMe, deep mesencephalic nuclei; Gi, gigantocellular reticular nucleus; GPe, Globus pallidus external segment; ic, internal capsule; IO, inferior olive; Pn, pontine nucleus; PnO, pontine reticular nucleus, oral part; py, medullary pyramid; pyd, pyramidal decussation; Rt, thalamic reticular nucleus; SC, superior colliculus; SN, substantia nigra; Str, striatum; VL, ventrolateral thalamic nucleus; VM, ventromedial thalamic nucleus.


Figure 15. Branching axons. (A) Cajal illustration () of primary axons entering the spinal cord and branching to innervate the spinal gray matter and brain areas. The red arrows indicate branch points. Thanks to Javier deFelipe for providing this image. (B) Schematic interpretation of A.


Figure 16. Comparison of conventional view (A) with the alternative view proposed here (B). The question marks in A indicate higher order thalamic relays, for which no specific function is suggested in this scheme. Further details in text. Abbreviations: FO, first order; HO, higher order.
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S. Murray Sherman. Functioning of Circuits Connecting Thalamus and Cortex. Compr Physiol 2017, 7: 713-739. doi: 10.1002/cphy.c160032