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Basal Ganglia—A Motion Perspective

Sten Grillner, Brita Robertson, Jeanette Hellgren Kotaleski

10.1002/cphy.c190045

Source: Volume 10, Issue 4, September 2020

Published online: September 2020

Full Article on Wiley Online Library



Abstract

The basal ganglia represent an ancient part of the nervous system that have remained organized in a similar way over the last 500 million years and are of importance for our ability to determine which actions to choose at any given moment in time. Salient or reward stimuli act via the dopamine system and contribute to motor or procedural learning (reinforcement learning). The input stage of the basal ganglia, the striatum, is shaped by glutamatergic input from the cortex and thalamus and by the dopamine system. All intrinsic neurons of the striatum are GABAergic and inhibitory except for the cholinergic interneurons. Too little dopamine and all vertebrates show symptoms similar to that of a Parkinsonian patient, whereas too much dopamine results in hyperkinesia with involuntary movements. In this article, we discuss the detailed organization of the basal ganglia, with the different cell types, their properties, and contributions to basal ganglia functions. The striatal projection neurons represent 95% of all neurons in the striatum and are subdivided into two types, one that projects directly to the output stage, referred to as the “direct” pathway that promotes action, and the other subtype that targets the output nuclei via intercalated basal ganglia nuclei. This “indirect” pathway has an opposite effect. The striatal projection neurons express a set of ion channels that give them a high threshold for activation, whereas neurons in all other parts of the basal ganglia have a resting discharge that allows for modulation in both an increased and decreased direction. © 2020 American Physiological Society. Compr Physiol 10:1241‐1275, 2020.

Figure 1. Figure 1. Common motor infrastructure from lamprey to man. Throughout the vertebrates, several basic motor behaviors are controlled by neuronal networks (CPGs) located in the brainstem and spinal cord. The basal ganglia play a crucial role in the selection of motor behaviors and are similarly organized in lamprey and primate. In primates, the addition of a well‐developed cerebral cortex provides a locus for networks controlling fine motor skills.
Figure 2. Figure 2. The basal ganglia subnuclei in the human brain. (A) The location of the different basal ganglia subnuclei at the level of thalamus. (B) A sagittal view of the brain showing the shape of the caudate‐putamen. (C) Schematic of the striatum indicating the matrix and striosome compartments.
Figure 3. Figure 3. The organization of the basal ganglia. The striatum consists of GABAergic neurons, as do GPe, GPi, and SNr. SNr and GPi represent the output level of the basal ganglia, and it projects via different subpopulations of neurons to the superior colliculus (SC), the mesencephalic (MLR), and diencephalic (DLR) locomotor command regions and other brainstem motor centers, as well as back to thalamus with efference copies of information sent to the brainstem. The dSPNs that target SNr/GPi express the dopamine D1 receptor (D1) and substance P (SP), while the iSPNs express the dopamine D2 receptor (D2) and enkephalin (Enk). The indirect loop is represented by the GPe, the STN, and the output level (SNr/GPi)—the net effect being an enhancement of activity in these nuclei. Also indicated is the dopamine input from the SNc (green) to striatum and brainstem centers. Excitatory glutamatergic neurons are shown in pink and GABAergic structures in blue color.
Figure 4. Figure 4. Striatal interneurons and the striatal microcircuit. (A) Each subtype of striatal interneurons identified by their neurotransmitter expression (inner circle), other molecular markers (middle circle), and electrophysiological properties (outer circle) are represented in the circular plot. Redrawn and modified, with permission, from Burke DA, et al., 2017 50, Figure 1. (B) The striatal microcircuit with the connectivity between the striatal projection neurons (SPNs) and their input from FS, LTS and ChIN interneurons. Abbreviations: ACh, acetylcholine; ChAT, choline‐acetyl transferase; ChIN, cholinergic interneuron; CR, calretinin; FA, fast adapting; FS, fast spiking; GABA, gamma‐butyric acid; 5‐HT3R, serotonin type‐3 receptor; LTS, low‐threshold spiking; NOS, nitric oxide synthase; NPY, neuropeptide Y; PV, parvalbumin; SOM, somatostatin; TAN, tonically active neurons; TH, tyrosine hydroxylase.
Figure 5. Figure 5. Input to different neuronal subpopulations in striatum. (A) Many cortical/pallial axons that target the brainstem and spinal cord (PT‐type) give off collaterals to neurons within the striatum. There is a subset of pyramidal neurons that have intratelencephalic axons projecting to the contralateral cortex/pallium (IT‐type) that also target the striatum. (B) Cortical and thalamic neurons target both direct and indirect striatal projection neurons (d/iSPNs) and the ChINs, FS, and LTS interneurons. The glutamatergic pedunculopontine (PPN) neurons only project to the interneurons, whereas the cholinergic PPN target the d/iSPNs. The red dashed arrow from cortex to ChINs indicates a variable and weak effect.
Figure 6. Figure 6. The direct, indirect, and hyperdirect pathways. Striatal projection neurons of the direct pathway (dSPNs) directly target the output level (SNr) and will enhance the excitability of brainstem motor targets through disinhibition and thus promote action. SPNs of the indirect pathway (iSPNs) will inhibit the spontaneously active GPe that in turn disinhibit SNr, thus increasing inhibition of downstream motor targets. The hyperdirect pathway projects to the glutamatergic STN that in turn targets SNr that will then inhibit the motor targets.
Figure 7. Figure 7. Connectivity of the globus pallidus externa (GPe) and the subthalamic nucleus (STN) with target structures. The GPe has two subpopulations of GABAergic cells, prototypical and arkypallidal cells. The prototypical cells receive input from iSPNs and STN. They project to the STN and GPi/SNr. The arkypallidal cells project back to the striatum's dSPNs, iSPNs, and interneurons, and receive input from the STN, cortex, and dSPNs. The STN receives input from the cortex, thalamus, PPN, SNc, and GPe. Like the GPe, the STN projects to the output nuclei GPi/SNr.
Figure 8. Figure 8. The activity of striatal projection neurons of the direct and indirect pathway during a goal‐directed push‐pull task. (A) Shows the activity pattern (spiking frequency) of a dSPN during a push/pull task. The red trace demonstrates a correct response (reward), and the blue trace an incorrect response (no reward). Upon the GO signal, the neuron is activated and remains active until a sound signals if the response will lead to a reward or not. The actual reward occurs with a further delay. Note that after the reward signal, the level of activity remains high, whereas with no reward the activity drops immediately. (B) The corresponding data for an indirect pathway neuron (iSPN). Note that immediately after the GO signal there is a marked increase of activity that rapidly decreases, while after the no‐reward signal there is a marked increase from base‐line. (C) Simplified scheme of the basal ganglia. Two separate populations of dSPNs and iSPNs control the push and the pull motion, respectively. The action is mediated by the basal ganglia output nuclei SNr and GPi to downstream motor circuits. Reused, with permission, from Grillner S, 2018 140.
Figure 9. Figure 9. The effects of enhanced or decreased dopamine activity on the direct and indirect pathways through the basal ganglia. (A) An enhanced dopamine activity excites the striatal projection neurons of the direct pathway that express dopamine receptors of the D1 subtype, while it inhibits those of the indirect pathway through their D2 receptors. (B) Illustrates the opposite situation with decreased dopamine activity that removes excitation from the direct pathway and reduces the inhibition of the indirect pathway and thereby indirectly increase the net excitation.
Figure 10. Figure 10. Parallel pathways for goal‐directed behavior conveyed via the head of the caudate nucleus (CDh) and habitual behavior produced through the tail of the caudate nucleus (CDt). The CDt and CDh receive input from different cortical regions and both target the superior colliculus to elicit saccadic eye movements, although through separate channels and via separate output neurons of the basal ganglia in Substantia Nigra pars reticulata (SNr). Moreover, separate parts of the Substantia Nigra pars compacta (SNc) supply the two circuits. Abbreviations: CDh, head of the caudate nucleus; CDt, tail of the caudate nucleus; c‐d‐l, caudal‐dorsal‐lateral; GPe(c), caudal part of GPe; GPe(r), rostral part of GPe; r‐v‐m, rostral‐ventral‐medial; SC, superior colliculus. Modified and redrawn, with permission, from Kim HF and Hikosaka O, 2015 183, Figure 6.
Figure 11. Figure 11. Schematic representation of the effect of an increased salient dopamine (DA) burst on striatal cell populations controlling different motor acts. When active, different cortical/thalamic cell populations (blue color) control the excitability of separate populations of striatal neurons, which are depolarized but not firing at the resting level of dopamine (2nd panel from the left). With enhanced DA activity, however, the striatal population becomes activated (3rd panel) and promotes motor action. The 4th panel shows the same condition for another population of striatal cells.
Figure 12. Figure 12. A sequence of tightly coupled discrete movements combined into one integrated movement, termed chunking. Illustration designed as in Figure 11, but with the addition of the salient dopamine burst that accompanies each discrete movement (see text).
Figure 13. Figure 13. Schematic representation of the excitatory globus pallidus projecting to the lateral habenulae (GPh; red), and the inhibitory compartment (GPi; blue) in lamprey, rodent, and primates. GPh and GPi are represented in separate nuclei in lamprey but are merged into two compartments within one nucleus (entopeduncular nucleus) in rodents. In primates, the habenular projecting parts are located mostly at the periphery, also referred to as the border region of the GPi. Modified, with permission, from Stephenson‐Jones M, et al., 2013 317, Figure 7.
Figure 14. Figure 14. Overview of the basal ganglia/habenular circuits underlying the control of motion and evaluation. The lower motion circuit corresponds to the circuits detailed in Figure 3. The dSPNs in the matrix compartment target GPi and SNr, as well as brainstem motor centers and send a collateral back to the thalamus (the lower part of the diagram). Also indicated is the indirect pathway via the GPe and STN. The evaluation circuit, in the upper part of the diagram, shows the lateral habenula (LHb) that target the dopamine (DA) neurons both directly and indirectly via the GABAergic rostromedial tegmental nucleus (RMTg). The LHb receives input from the glutamatergic habenula‐projecting globus pallidus (GPh). The GPh receives excitation from cortex and thalamus, whereas it receives inhibition from iSPNs in the striosome compartment. DA neurons are inhibited by striosomal dSPNs and send projections to the mesencephalic locomotor region (MLR) and optic tectum. The color code is blue for GABAergic, red for glutamatergic, and green for dopaminergic neurons.
Figure 15. Figure 15. Receptor‐induced signaling activating downstream effectors important for long‐term potentiation (LTP) or depression (LTD). Activation of different receptors activates different protein kinases involved in LTP, whereas other sets of receptors have other downstream targets and evoke LTD. There is evidence that eliciting of LTP processes inhibit LTD, and vice versa. CaMKII, Ca2+/calmodulin‐dependent protein kinase II; PKA, protein kinase A; PKC, protein kinase C; PKG, protein kinase G; NO, nitric oxide; 2AG, 2‐arachidonoylglycerol (an endocannabinoid); ERK, extracellular signal‐regulated kinases; sGC, soluble guanylyl cyclase; mGluR, metabotropic glutamate receptor; A2AR, adenosine 2A receptor.
Figure 16. Figure 16. The characteristic motor symptoms of Parkinson's disease. Front and side views of a man portrayed with Parkinson's disease. These are woodcut reproductions. From Paul de Saint‐Leger's 1879 doctoral thesis, Paralysie agitante. Fig. 145) published by Gowers 128, p. 591.
Figure 17. Figure 17. Data‐driven detailed simulation of striatum. (A) Shows the somata of the number of cells (71,242) contained in 1 mm3, distributed according to estimated densities. (B) Shows a limited number of cells with their somatodendritic arbor, based on detailed reconstruction of SPNs of both types, ChINs, and FS and LTS interneurons. The high density of dendritic and axonal branches within the tissue is evident. For each type of cell, the detailed membrane properties are simulated and validated versus their biological counterparts. (C) Simulated cells with dendrites are shown with different magnification from left to right. A touch detection algorithm is used to detect where axonal and dendritic structures come close (red circles as indicated). Depending on the pre‐ and postsynaptic cell types, adjusted pruning rules are applied and validated against established connectivity. In this way, the neuronal microstructure is reconstructed bottom‐up in a data‐driven manner. Also, optimization algorithms are used to fit electrophysiological properties to the different neuronal types. These data‐driven workflows have also been used to predict cortical microcircuits 151,225.
Figure 18. Figure 18. Phylogenetic tree of vertebrates. The lamprey diverged from the line to mammals around 560 million years ago (mya). Adapted, with permission, from Reiner A, et al., 1998 289.
Figure 19. Figure 19. From lamprey to primates—the organization of the basal ganglia is almost identical throughout vertebrate phylogeny. (A) The striatum consists of GABAergic neurons (blue), as do the GPe, GPi, and SNr. The output level of the basal ganglia is represented by the GPi/SNr, and it projects via different subpopulations of neurons to the optic tectum (superior colliculus in mammals), the mesencephalic (MLR) and diencephalic (DLR) locomotor command regions and other brainstem motor centers, and send additional efference copies of the information back to thalamus. The indirect loop is represented by the GPe, the STN, and the output level (SNr/GPi)—the net effect is an enhancement of activity in these nuclei. The dSPNs of the direct pathway express the dopamine D1 receptor and substance P (SP), while the iSPNs express the dopamine D2 receptor and enkephalin (Enk). Excitatory glutamatergic neurons are represented by pink, GABAergic structures in blue and dopamine input from the SNc in green. (B) A table showing the key features of the basal ganglia organization that are found in mammals and lamprey. So far, subtypes of FS striatal interneurons have not been demonstrated in the lamprey.
Figure 20. Figure 20. The SNc connectome in lamprey and mammals. The efferent and afferent connectivity of the SNc is virtually identical in lamprey and mammals. Thus, the dopaminergic neurons within SNc project to the same structures in the basal ganglia as in mammals and the same midbrain motor centers. The input to SNc is similarly identical from the striatum, STN, cortex/pallium, PPN, and the lateral habenulae. Reused, with permission, from Perez‐Fernandez J, et al., 2014 271.
Figure 21. Figure 21. Scheme summarizing the main building‐blocks promoting and inhibiting action in the forebrain. Cortical circuits can directly and via the direct pathway promote action, as can thalamic circuits and the dopamine system. The cerebral cortex can also inhibit action via the STN, the hyperdirect pathway, and via the striatum and the indirect pathway and finally via GPe inhibition of striatum. For simplicity the output nuclei of the basal ganglia are not included—only the net effect of the direct and indirect pathway.


Figure 1. Common motor infrastructure from lamprey to man. Throughout the vertebrates, several basic motor behaviors are controlled by neuronal networks (CPGs) located in the brainstem and spinal cord. The basal ganglia play a crucial role in the selection of motor behaviors and are similarly organized in lamprey and primate. In primates, the addition of a well‐developed cerebral cortex provides a locus for networks controlling fine motor skills.


Figure 2. The basal ganglia subnuclei in the human brain. (A) The location of the different basal ganglia subnuclei at the level of thalamus. (B) A sagittal view of the brain showing the shape of the caudate‐putamen. (C) Schematic of the striatum indicating the matrix and striosome compartments.


Figure 3. The organization of the basal ganglia. The striatum consists of GABAergic neurons, as do GPe, GPi, and SNr. SNr and GPi represent the output level of the basal ganglia, and it projects via different subpopulations of neurons to the superior colliculus (SC), the mesencephalic (MLR), and diencephalic (DLR) locomotor command regions and other brainstem motor centers, as well as back to thalamus with efference copies of information sent to the brainstem. The dSPNs that target SNr/GPi express the dopamine D1 receptor (D1) and substance P (SP), while the iSPNs express the dopamine D2 receptor (D2) and enkephalin (Enk). The indirect loop is represented by the GPe, the STN, and the output level (SNr/GPi)—the net effect being an enhancement of activity in these nuclei. Also indicated is the dopamine input from the SNc (green) to striatum and brainstem centers. Excitatory glutamatergic neurons are shown in pink and GABAergic structures in blue color.


Figure 4. Striatal interneurons and the striatal microcircuit. (A) Each subtype of striatal interneurons identified by their neurotransmitter expression (inner circle), other molecular markers (middle circle), and electrophysiological properties (outer circle) are represented in the circular plot. Redrawn and modified, with permission, from Burke DA, et al., 2017 50, Figure 1. (B) The striatal microcircuit with the connectivity between the striatal projection neurons (SPNs) and their input from FS, LTS and ChIN interneurons. Abbreviations: ACh, acetylcholine; ChAT, choline‐acetyl transferase; ChIN, cholinergic interneuron; CR, calretinin; FA, fast adapting; FS, fast spiking; GABA, gamma‐butyric acid; 5‐HT3R, serotonin type‐3 receptor; LTS, low‐threshold spiking; NOS, nitric oxide synthase; NPY, neuropeptide Y; PV, parvalbumin; SOM, somatostatin; TAN, tonically active neurons; TH, tyrosine hydroxylase.


Figure 5. Input to different neuronal subpopulations in striatum. (A) Many cortical/pallial axons that target the brainstem and spinal cord (PT‐type) give off collaterals to neurons within the striatum. There is a subset of pyramidal neurons that have intratelencephalic axons projecting to the contralateral cortex/pallium (IT‐type) that also target the striatum. (B) Cortical and thalamic neurons target both direct and indirect striatal projection neurons (d/iSPNs) and the ChINs, FS, and LTS interneurons. The glutamatergic pedunculopontine (PPN) neurons only project to the interneurons, whereas the cholinergic PPN target the d/iSPNs. The red dashed arrow from cortex to ChINs indicates a variable and weak effect.


Figure 6. The direct, indirect, and hyperdirect pathways. Striatal projection neurons of the direct pathway (dSPNs) directly target the output level (SNr) and will enhance the excitability of brainstem motor targets through disinhibition and thus promote action. SPNs of the indirect pathway (iSPNs) will inhibit the spontaneously active GPe that in turn disinhibit SNr, thus increasing inhibition of downstream motor targets. The hyperdirect pathway projects to the glutamatergic STN that in turn targets SNr that will then inhibit the motor targets.


Figure 7. Connectivity of the globus pallidus externa (GPe) and the subthalamic nucleus (STN) with target structures. The GPe has two subpopulations of GABAergic cells, prototypical and arkypallidal cells. The prototypical cells receive input from iSPNs and STN. They project to the STN and GPi/SNr. The arkypallidal cells project back to the striatum's dSPNs, iSPNs, and interneurons, and receive input from the STN, cortex, and dSPNs. The STN receives input from the cortex, thalamus, PPN, SNc, and GPe. Like the GPe, the STN projects to the output nuclei GPi/SNr.


Figure 8. The activity of striatal projection neurons of the direct and indirect pathway during a goal‐directed push‐pull task. (A) Shows the activity pattern (spiking frequency) of a dSPN during a push/pull task. The red trace demonstrates a correct response (reward), and the blue trace an incorrect response (no reward). Upon the GO signal, the neuron is activated and remains active until a sound signals if the response will lead to a reward or not. The actual reward occurs with a further delay. Note that after the reward signal, the level of activity remains high, whereas with no reward the activity drops immediately. (B) The corresponding data for an indirect pathway neuron (iSPN). Note that immediately after the GO signal there is a marked increase of activity that rapidly decreases, while after the no‐reward signal there is a marked increase from base‐line. (C) Simplified scheme of the basal ganglia. Two separate populations of dSPNs and iSPNs control the push and the pull motion, respectively. The action is mediated by the basal ganglia output nuclei SNr and GPi to downstream motor circuits. Reused, with permission, from Grillner S, 2018 140.


Figure 9. The effects of enhanced or decreased dopamine activity on the direct and indirect pathways through the basal ganglia. (A) An enhanced dopamine activity excites the striatal projection neurons of the direct pathway that express dopamine receptors of the D1 subtype, while it inhibits those of the indirect pathway through their D2 receptors. (B) Illustrates the opposite situation with decreased dopamine activity that removes excitation from the direct pathway and reduces the inhibition of the indirect pathway and thereby indirectly increase the net excitation.


Figure 10. Parallel pathways for goal‐directed behavior conveyed via the head of the caudate nucleus (CDh) and habitual behavior produced through the tail of the caudate nucleus (CDt). The CDt and CDh receive input from different cortical regions and both target the superior colliculus to elicit saccadic eye movements, although through separate channels and via separate output neurons of the basal ganglia in Substantia Nigra pars reticulata (SNr). Moreover, separate parts of the Substantia Nigra pars compacta (SNc) supply the two circuits. Abbreviations: CDh, head of the caudate nucleus; CDt, tail of the caudate nucleus; c‐d‐l, caudal‐dorsal‐lateral; GPe(c), caudal part of GPe; GPe(r), rostral part of GPe; r‐v‐m, rostral‐ventral‐medial; SC, superior colliculus. Modified and redrawn, with permission, from Kim HF and Hikosaka O, 2015 183, Figure 6.


Figure 11. Schematic representation of the effect of an increased salient dopamine (DA) burst on striatal cell populations controlling different motor acts. When active, different cortical/thalamic cell populations (blue color) control the excitability of separate populations of striatal neurons, which are depolarized but not firing at the resting level of dopamine (2nd panel from the left). With enhanced DA activity, however, the striatal population becomes activated (3rd panel) and promotes motor action. The 4th panel shows the same condition for another population of striatal cells.


Figure 12. A sequence of tightly coupled discrete movements combined into one integrated movement, termed chunking. Illustration designed as in Figure 11, but with the addition of the salient dopamine burst that accompanies each discrete movement (see text).


Figure 13. Schematic representation of the excitatory globus pallidus projecting to the lateral habenulae (GPh; red), and the inhibitory compartment (GPi; blue) in lamprey, rodent, and primates. GPh and GPi are represented in separate nuclei in lamprey but are merged into two compartments within one nucleus (entopeduncular nucleus) in rodents. In primates, the habenular projecting parts are located mostly at the periphery, also referred to as the border region of the GPi. Modified, with permission, from Stephenson‐Jones M, et al., 2013 317, Figure 7.


Figure 14. Overview of the basal ganglia/habenular circuits underlying the control of motion and evaluation. The lower motion circuit corresponds to the circuits detailed in Figure 3. The dSPNs in the matrix compartment target GPi and SNr, as well as brainstem motor centers and send a collateral back to the thalamus (the lower part of the diagram). Also indicated is the indirect pathway via the GPe and STN. The evaluation circuit, in the upper part of the diagram, shows the lateral habenula (LHb) that target the dopamine (DA) neurons both directly and indirectly via the GABAergic rostromedial tegmental nucleus (RMTg). The LHb receives input from the glutamatergic habenula‐projecting globus pallidus (GPh). The GPh receives excitation from cortex and thalamus, whereas it receives inhibition from iSPNs in the striosome compartment. DA neurons are inhibited by striosomal dSPNs and send projections to the mesencephalic locomotor region (MLR) and optic tectum. The color code is blue for GABAergic, red for glutamatergic, and green for dopaminergic neurons.


Figure 15. Receptor‐induced signaling activating downstream effectors important for long‐term potentiation (LTP) or depression (LTD). Activation of different receptors activates different protein kinases involved in LTP, whereas other sets of receptors have other downstream targets and evoke LTD. There is evidence that eliciting of LTP processes inhibit LTD, and vice versa. CaMKII, Ca2+/calmodulin‐dependent protein kinase II; PKA, protein kinase A; PKC, protein kinase C; PKG, protein kinase G; NO, nitric oxide; 2AG, 2‐arachidonoylglycerol (an endocannabinoid); ERK, extracellular signal‐regulated kinases; sGC, soluble guanylyl cyclase; mGluR, metabotropic glutamate receptor; A2AR, adenosine 2A receptor.


Figure 16. The characteristic motor symptoms of Parkinson's disease. Front and side views of a man portrayed with Parkinson's disease. These are woodcut reproductions. From Paul de Saint‐Leger's 1879 doctoral thesis, Paralysie agitante. Fig. 145) published by Gowers 128, p. 591.


Figure 17. Data‐driven detailed simulation of striatum. (A) Shows the somata of the number of cells (71,242) contained in 1 mm3, distributed according to estimated densities. (B) Shows a limited number of cells with their somatodendritic arbor, based on detailed reconstruction of SPNs of both types, ChINs, and FS and LTS interneurons. The high density of dendritic and axonal branches within the tissue is evident. For each type of cell, the detailed membrane properties are simulated and validated versus their biological counterparts. (C) Simulated cells with dendrites are shown with different magnification from left to right. A touch detection algorithm is used to detect where axonal and dendritic structures come close (red circles as indicated). Depending on the pre‐ and postsynaptic cell types, adjusted pruning rules are applied and validated against established connectivity. In this way, the neuronal microstructure is reconstructed bottom‐up in a data‐driven manner. Also, optimization algorithms are used to fit electrophysiological properties to the different neuronal types. These data‐driven workflows have also been used to predict cortical microcircuits 151,225.


Figure 18. Phylogenetic tree of vertebrates. The lamprey diverged from the line to mammals around 560 million years ago (mya). Adapted, with permission, from Reiner A, et al., 1998 289.


Figure 19. From lamprey to primates—the organization of the basal ganglia is almost identical throughout vertebrate phylogeny. (A) The striatum consists of GABAergic neurons (blue), as do the GPe, GPi, and SNr. The output level of the basal ganglia is represented by the GPi/SNr, and it projects via different subpopulations of neurons to the optic tectum (superior colliculus in mammals), the mesencephalic (MLR) and diencephalic (DLR) locomotor command regions and other brainstem motor centers, and send additional efference copies of the information back to thalamus. The indirect loop is represented by the GPe, the STN, and the output level (SNr/GPi)—the net effect is an enhancement of activity in these nuclei. The dSPNs of the direct pathway express the dopamine D1 receptor and substance P (SP), while the iSPNs express the dopamine D2 receptor and enkephalin (Enk). Excitatory glutamatergic neurons are represented by pink, GABAergic structures in blue and dopamine input from the SNc in green. (B) A table showing the key features of the basal ganglia organization that are found in mammals and lamprey. So far, subtypes of FS striatal interneurons have not been demonstrated in the lamprey.


Figure 20. The SNc connectome in lamprey and mammals. The efferent and afferent connectivity of the SNc is virtually identical in lamprey and mammals. Thus, the dopaminergic neurons within SNc project to the same structures in the basal ganglia as in mammals and the same midbrain motor centers. The input to SNc is similarly identical from the striatum, STN, cortex/pallium, PPN, and the lateral habenulae. Reused, with permission, from Perez‐Fernandez J, et al., 2014 271.


Figure 21. Scheme summarizing the main building‐blocks promoting and inhibiting action in the forebrain. Cortical circuits can directly and via the direct pathway promote action, as can thalamic circuits and the dopamine system. The cerebral cortex can also inhibit action via the STN, the hyperdirect pathway, and via the striatum and the indirect pathway and finally via GPe inhibition of striatum. For simplicity the output nuclei of the basal ganglia are not included—only the net effect of the direct and indirect pathway.
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Article Title: Basal Ganglia—A Motion Perspective
 

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Sten Grillner, Brita Robertson, Jeanette Hellgren Kotaleski. Basal Ganglia—A Motion Perspective. Compr Physiol 2020, 10: 1241-1275. doi: 10.1002/cphy.c190045