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Link to original content: https://pubmed.ncbi.nlm.nih.gov/20850966
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Review
. 2010 Dec;20(6):704-16.
doi: 10.1016/j.conb.2010.08.022. Epub 2010 Sep 17.

Basal ganglia contributions to motor control: a vigorous tutor

Robert S Turner  1 , Michel Desmurget
Affiliations
Review

Basal ganglia contributions to motor control: a vigorous tutor

Robert S Turner et al. Curr Opin Neurobiol. 2010 Dec.

Abstract

The roles of the basal ganglia (BG) in motor control are much debated. Many influential hypotheses have grown from studies in which output signals of the BG were not blocked, but pathologically disturbed. A weakness of that approach is that the resulting behavioral impairments reflect degraded function of the BG per se mixed together with secondary dysfunctions of BG-recipient brain areas. To overcome that limitation, several studies have focused on the main skeletomotor output region of the BG, the globus pallidus internus (GPi). Using single-cell recording and inactivation protocols these studies provide consistent support for two hypotheses: the BG modulates movement performance ('vigor') according to motivational factors (i.e. context-specific cost/reward functions) and the BG contributes to motor learning. Results from these studies also add to the problems that confront theories positing that the BG selects movement, inhibits unwanted motor responses, corrects errors on-line, or stores and produces well-learned motor skills.

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Figures

Figure 1
Figure 1
Disconnection of the BG skeletomotor circuit does not impair movement initiation or performance of an overlearned motor sequence, but selectively affects movement speed and extent. Animals moved a joystick (a, top) through a series of four out-and-back component movements ((b-d) red, blue, green, and cyan traces, respectively) before and after an injection of muscimol (a long-acting GABAergic inhibitory agent) into the GPi. (a, bottom) illustrates sites of injections (letters) in a typical coronal plane through GPe and GPi. Performance is illustrated for single trials under the Random pre-injection (b), OverLearned pre-injection (c) and OverLearned post-injection (d) conditions. The left and right panel show position and velocity data, respectively. Black sections of the velocity curves indicate periods of immobility (velocity<25-mm/s). Left: Continuous arcs in corners indicate positions of the instruction cues. Dotted arcs indicate the peripheral target zones for cursor movements. Right: Dots on the velocity curves indicate the instant of presentation of the instruction cue. Under the OverLearned condition (c), outward movements to capture a peripheral target were often anticipatory, beginning before the instruction cue was presented, and this anticipatory performance persisted post-injection (d). Numbers define targets (left) and which target was indicated by each instruction cue (right). The figures are scaled to show the central region of the workspace. (e) Inactivations had a negligible effect on reaction times [RTs; left, compare pre-injection (open symbols) versus post-injection means (filled symbols)]. This was true irrespective of whether animals performed OverLearned sequences or Random sequences, or whether the target to capture was indicated by a cue’s spatial location (circles) or its color (triangles). In contrast, muscimol injections consistently reduced movement velocity (middle) and extent (right) under all conditions. Symbols indicate means±SEM from 19 separate injections of muscimol into the contralateral GPi of two animals. (Fig. 1b-d is from [55••] used with permission from the Society for Neuroscience. Fig. 1e is adapted from [109].)
Figure 2
Figure 2
Activity in skeletomotor regions of the BG correlates closely with movement gain (extent and velocity). (a) Healthy human subjects performed a continuous visuo-manual tracking task by moving a hand-held joystick (black traces illustrate representative performance of one subject) to follow constant-velocity displacements of an on-screen target (gray traces). The extent and velocity of hand movements differed between scans by training subjects during periods between scans on one of four different joystick-to-cursor scaling factors. (b) Areas of increasing cerebral blood flow (CBF) with increasing movement gain are shown in orange-yellow (P<0.001 uncorrected). Significant changes were identified at only three sites: left dorsal putamen (upper panel), right dorsal putamen (middle panel), and right cerebellum (lower panel). (c) Brain activity (normalized CBF mean±SEM) increased monotonically with movement extent at the identified sites in the BG and cerebellum. (Adapted from [71] with copyright permission from the American Physiological Society.)
Figure 3
Figure 3
Disconnection of the BG homologue in the songbird blocks the expression of newly-acquired song adaptive changes. (a) The bird anterior forebrain pathway (AFP) contains homologues to most structures of the mammalian BG. Output from the AFP affects motor execution pathways via the premotor-like LMAN nucleus. Andalman et al. [11••] perturbed singing selectively using a head-mounted microphone and speaker system. (b) White noise perturbations were delivered when the fundamental frequency of one song syllable (“Targeted region”) crossed a specific pitch threshold (red vertical lines, middle panel). The white noise burst grossly altered the song heard by the animal (bottom). On different days, the noise perturbation either targeted pitches above the mean syllable frequency (“Down days”, illustrated in (b)) or pitches below the mean (“Up days”, not shown). (c) Tetrodotoxin (TTX) was infused into LMAN bilaterally using the reverse microdialysis technique. (d) Before TTX infusion, animals responded to noise perturbations by progressively changing the fundamental frequency of the targeted syllable so as to avoid the perturbation. TTX infusion resulted in an immediate loss of that adaptive change. (e) Infusion of vehicle alone had no effect on noise-avoiding adaptive changes. (f-g) TTX infusions caused rapid maladaptive changes in the targeted syllable’s fundamental frequency (i.e., an increase in pitch on “Down days” and a decrease on “Up days”). (Adapted from Figures 1 and 2 of [11••] with permission from the authors and the National Academy of Sciences.)
Box 1 Figure
Box 1 Figure
Circuit diagrams of the BG and associated input–output connections. (a) The positions of key BG structures involved in skeletomotor control and their basic input-output connectivity superimposed on a parasagittal section through the macaque brain. The basic loop circuit includes an excitatory glutamatergic (Glu) projection from the neocortex to the striatum (caudate nucleus and putamen) and then inhibitory (γ-amino butyric acid-containing; GABAergic) striatal projection (the ‘direct pathway’) to the internal globus pallidum (GPi). GABAergic neurons in GPi project to targets in the thalamus and brainstem. The main thalamic target of this circuit (VA/VL, ventral anterior/ventrolateral nucleus of the thalamus) projects to the frontal cortex including parts of the premotor and primary motor cortex. (b) Internal connectivity of the BG motor circuit (front sub-panel) showing principal pathways only. Direct and indirect pathways start in projection neurons of the putamen (part of the striatum) that express D1- and D2-type dopamine receptors, respectively. D2-type neurons project to the external globus pallidus (GPe). GPe projects to the subthalamic nucleus (STN) and GPi. STN also receives monosynaptic Glu input from the motor cortices and projects to GPi and GPe. GPi sends GABAergic projections to VA/VL and the centre median–parafascicular intralaminar complex (CMPf) of the thalamus. CMPf closes another loop by projecting back to the striatum. GPi also projects to brainstem regions such as the pedunculopontine nucleus. Dopaminergic (DA) neurons of the substantia nigra pars compacta (SNc) innervate the striatum and, less densely, the GP and STN. Successive subpanels represent the parallel BG circuits that sub-serve oculomotor, associative, and limbic functions. Note that these circuits pass through anatomically-distinct regions at each stage, including different regions of the STN and thalamus (not shown in figure).
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References

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