A Theory of the Basal Ganglia and Their Disorders (Conceptual Advances in Brain Research)
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Importantly, the anterior and posterior parts of the basal ganglia work separately for the initial learning and the later skillful performance. After his return to NEI, Hikosaka extended his research on the basal ganglia and related brain areas. He demonstrated that dopamine neurons function differently in different areas of the basal ganglia — findings that upended the then-existing view of the role of dopamine neurons in emotion and motivation. In recent years Hikosaka found that old reward histories create long-term value memories of many objects and that animals are automatically attracted by the historically good objects.
This behavior is controlled selectively by the very posterior part of the basal ganglia tail of the caudate nucleus — substantia nigra pars reticulata — superior colliculus. Wolfram Schultz, MD, of the University of Cambridge, has revolutionized the concept of how reward information is processed in the brain. In a now-classic series of experiments conducted in the s and s, Schultz demonstrated that when animals receive a reward, dopamine neurons in a brain area known as the basal ganglia send a signal that causes the release of the neurotransmitter.
Social brain dysfunctions in patients with Parkinson’s disease: a review of theory of mind studies
He also showed that the neural pattern of the activity changes as the animals learn how to respond to receive the reward — and that learned cues can trigger changes even in the absence of a reward. In further experiments, he identified and described reward-response neurons in additional brain structures, including the orbitofrontal cortex, striatum and amygdala.
Through these and other pioneering studies, Schultz demonstrated how theory and experiment could be linked, thus dramatically influencing subsequent research on reward and choice. More recently, Schultz has focused his research on uniting prediction error concepts from animal learning theory with economic utility theory, finding strong evidence suggesting that the dopamine response is related to the concept of utility. Those discoveries are transforming both experimental and theoretical research in the relatively new field of neuroeconomics. Note: material may have been edited for length and content.
It has also deepened our understanding of a wide range of neurodegenerative and neuropsychiatric disorders in which the basal ganglia and behavioral control is compromised. She then followed this transformative discovery with studies describing the functionally of that architecture, including the finding that changes in striatal neural activity during the learning process lead to the formation of pathological habits, such as those that characterize obsessive compulsive disorder.
In his landmark research, Hikosaka identified the basal ganglia circuitry involved in saccadic voluntary eye movements and then went on to make further discoveries that described the importance of this circuitry in memory, motor behavior and reward — findings that opened up exciting new avenues of research into the study of motivation.
He demonstrated that dopamine neuronal signals within the basal ganglia are directly related to reward prediction errors, which are thought to be the key signal needed to drive reward-related learning. Graybiel, PhD, of the McGovern Institute for Brain Research at the Massachusetts Institute of Technology MIT , pioneered our understanding of the important role that basal ganglia, a group of nuclei clusters of neurons deep within the forebrain, play in a wide range of neurological disorders. At the time she started her research, in the s, most scientists were ignoring that area of the brain.
Graybiel, however, persevered. In a groundbreaking experiment, she found that the striatum, the largest nucleus within the basal ganglia, was not a homogenous mass of cells as was commonly believed at the time. Instead, it had a distinct and sophisticated architecture with column-like modules — dubbed striosomes by Graybiel — that distributed nearly every known neurotransmitter. She also found that striosomes were surrounded by a matrix, which was itself modular.
In an extraordinary series of subsequent experiments, Graybiel went on to demonstrate the functionality of this architecture. The basal ganglia are one of the fundamental processing units of the mammalian brain. Progressive degeneration of one of their major components, the ascending dopamine projection to the striatum, is a central pathological feature of Parkinson's disease.
Imaging and post-mortem investigations reveal that degeneration of the dopamine projection is uneven in most cases, with input to caudolateral sectors of the putamen most severely affected. In the animal learning literature an important distinction has been forged between goal-directed and habitual control of behaviour. When behaviour is goal-directed, action selection is determined by the relative utility of predicted outcomes, whereas habits are under stimulus control and largely independent of outcome value. A seminal series of investigations in rodents by Balleine and colleagues established that the dorsomedial associative territories of the striatum are crucial for goal-directed control, whereas laterally located sensorimotor territories are essential for habits.
Formal behavioural tests for example, outcome devaluation were used to determine whether an observed behaviour for example, pressing a lever was under goal-directed or habitual control. Recent neuroimaging studies using the same formal tests suggest that a similar spatial segregation of goal-directed and habitual control is present within the human striatum.
As the loss of dopamine in Parkinson's disease is predominantly from the caudolateral sensorimotor territories, we would expect patients to experience major deficits in their production of habits. Because the same behavioural output can be directed by processing in spatially segregated regions of the basal ganglia, it must be assumed that the efferent projections of goal-directed and habitual control circuits must at some point converge on the 'final common motor path'.
Given that the loss of dopamine in the basal ganglia is associated with enhanced oscillatory and inhibitory outputs, we suggest that for goal-directed control to be expressed, the distorting inhibitory signals from the habit system must be overcome at the point where the goal-directed and habitual control circuits converge. We conclude by reviewing evidence suggesting that many of the behavioural difficulties experienced by patients with Parkinson's disease can be interpreted in terms of an impaired automatic control of normal habits, coupled with distorting inhibitory influences imposed on the expression of residual goal-directed behaviours.
In the light of this analysis, future work will need to establish how far the reported cognitive deficits in Parkinson's disease are due to the primary disease state additional loss of dopamine from goal-directed circuits or are a result of goal-directed control being overwhelmed by the absence of automatic control routines that are normally provided by the stimulus—response habit systems.
Ferrier, D. Penney, J. Striatal inhomogeneities and basal ganglia function. Albin, R. The functional anatomy of basal ganglia disorders. Trends Neurosci. Chevalier, G. Disinhibition as a basic process in the expression of striatal functions. This review introduced a conceptual development in suggesting that a pause in neuronal firing in basal ganglia output nuclei disinhibits efferent targets and is the major physiological mechanism by which the basal ganglia exert their effects on behaviour.
Gerfen, C. DeLong, M. Primate models of movement disorders of basal ganglia origin. A classic review of the basal ganglia pathophyisiological model and the concepts on which it is based. D1 and D2 dopamine receptor regulated gene expression of striatonigral and striatopallidal neurons. Science , — Crossman, A. Primate models of dyskinesia: the experimental approach to the study of basal ganglia-related involuntary movement disorders. Neuroscience 21 , 1—40 Bevan, M.
Convergent synaptic input from the neostriatum and the subthalamus onto identified nigrothalamic neurons in the rat. Redgrave, P. Basal ganglia. Scholarpedia 2 , Wu, Y. The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Matamales, M. Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice.
Hartmann-von Monakow, K. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Brain Res. Nambu, A. Functional significance of the cortico—subthalamo—pallidal 'hyperdirect' pathway. Lanciego, J. Thalamic innervation of striatal and subthalamic neurons projecting to the rat entopeduncular nucleus. Feger, J. The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations — a comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study.
Neuroscience 60 , — Coizet, V. Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. Mena-Segovia, J. Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Smith, Y. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86 , — Miwa, H.
Subthalamo-pallido-striatal axis: a feedback system in the basal ganglia. Neuroreport 12 , — Shink, E. The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 73 , — Kita, H. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. Monkey globus pallidus external segment neurons projecting to the neostriatum. Neuroreport 10 , — McGeorge, A. The organization of the projection from the cerebral cortex to the striatum in the rat.
Neuroscience 29 , — Romanelli, P. Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels. Wiesendanger, E. Topography of cortico-striatal connections in man: anatomical evidence for parallel organization. Nakano, K. Neural circuits and functional organization of the striatum.
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Alexander, G. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. The classic and first description of the re-entrant looped architecture by which the basal ganglia interact with external structures. McHaffie, J. Subcortical loops through the basal ganglia. Bolam, J. Landes Co. Gillies, A. Models of the subthalamic nucleus: the importance of intranuclear connectivity. Benarroch, E. Subthalamic nucleus and its connections: anatomic substrate for the network effects of deep brain stimulation.
Neurology 70 , — Parent, M. The microcircuitry of primate subthalamic nucleus. Parkinsonism Relat. Neural circuits and topographic organization of the basal ganglia and related regions. Brain Dev. Voorn, P.
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Putting a spin on the dorsal-ventral divide of the striatum. Draganski, B. Evidence for segregated and integrative connectivity patterns in the human basal ganglia. Lehericy, S. Cortex 14 , — Doron, O. Evidence for asymmetric intra substantia nigra functional connectivity-application to basal ganglia processing. Neuroimage 49 , — Krout, K. Brainstem projections to midline and intralaminar thalamic nuclei of the rat.
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Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. Erro, E. Relationships between thalamostriatal neurons and pedunculopontine projections to the thalamus: a neuroanatomical tract-tracing study in the rat. Bjorklund, A. Dopamine neuron systems in the brain: an update. Matsuda, W. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum.
Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey. Cragg, S. Synaptic release of dopamine in the subthalamic nucleus. Grace, A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41 , 1—24 The basal ganglia: a vertebrate solution to the selection problem?
Neuroscience 89 , — A general description of the mechanisms and computational requirements of selection performed by the basal ganglia. Mink, J. The basal ganglia: focused selection and inhibition of competing motor programs. Hikosaka, O. Role of the basal ganglia in the control of purposive saccadic eye movements. The short-latency dopamine signal: a role in discovering novel actions?
Nature Rev. What is reinforced by phasic dopamine signals? Schultz, W. Behavioral theories and the neurophysiology of reward. Microstimulation of the primate neurostriatum. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. Kimura, M. Behaviorally contingent property of movement-related activity of the primate putamen. Flaherty, A. Two input systems for body representation in the primate striatal matrix: experimental evidence in the squirrel monkey.
Functional properties of monkey caudate neurons.
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Activities related to saccadic eye movements. Functional properties of monkey caudate neurons II. Visual and auditory responses. Tremblay, L. Modifications of reward expectation-related neuronal activity during learning in primate striatum.
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Scholz, V. Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks. Gerardin, E. Foot, hand, face and eye representation in the human striatum. Cortex 13 , — Dickinson, A. The 28th Bartlett Memorial Lecture Causal learning: an associative analysis. Balleine, B. The integrative function of the basal ganglia in instrumental conditioning. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35 , 48—69 This paper provides well-written and clearly explained views about the role of the basal ganglia in the control of human and rodent behaviour.
Yin, H. The role of the basal ganglia in habit formation. An excellent review of the role of the basal ganglia in habitual and goal-directed control.