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basal ganglia

basal ganglia In classical neuroanatomy this terms refers to the masses of grey matter lying deeply within each cerebral hemisphere, separated from the outer shell of cerebral cortex by a wide band of white matter. Together these large aggregations of nerve cells or ‘nuclei’ are described as the ‘striate body’ (corpus striatum — striped because it is partly split by bands of white matter). However as a result of much clinical and animal-based basic research, other structures lower in the brain are now included with the basal ganglia on a functional basis, notably the subthalamic nuclei and the substantia nigra.

A rich variety of chemical transmitters was identified within the basal ganglia, and sophisticated anatomical tracing techniques employing radioactive or fluorescent ‘tracers’ to mark out nerve pathways, soon disclosed that they receive information from throughout the frontal lobe cerebral cortex in addition to the motor cortex and frontal eye fields, and also from the substantia nigra in the uppermost part of the brainstem. Moreover, it was shown that the darkly staining neuronal cell bodies of the substantia nigra, responsible for its name, contained the neurotransmitter dopamine, and that the number of these neurons was severely reduced in the brains of patients who were suffering from Parkinsonism at the time of death. Furthermore, dopamine, and other transmitters such as noradrenaline and serotonin, were found to be depleted also in the basal ganglia of these same patients. These observations and the clues they provided to the functional links between these structures led to the remarkable twentieth-century discovery that the substance L-DOPA, the metabolic precursor of dopamine, when given orally in adequate quantities, was very effective in diminishing or abolishing the disabling tremor of what in earlier times was called ‘the shaking palsy’. This localization of the site of the problem promoted more research based on stereotactic surgery (three-dimensional positioning of micro-surgical instruments) which, when combined with electrophysiological and imaging procedures, has greatly benefitted patients so severely disabled by tremor that the surgical relief of symptoms has been necessary. Another feature of Parkinson's disease is ‘akinesis’ — paucity of movement and slowness in starting or finishing movements. Although initiated by an act of will, most movements are carried out automatically; they are implemented through motor programmes refined by practice throughout life. This is the domain that the basal ganglia appear to be involved in. Crucial to this is the fact that the output from the basal ganglia is not only passed to brain stem centres and relayed on to the spinal cord; it also reaches the areas of the thalamus that transmit information back to the cerebral cortex, as well as mediating the control of automated movement by the cerebellum. Still more recent research indicates that this system does not simply function by processing the signal flow in a serial mechanism (as suggested by the classical anatomical studies of connectivity between the cortex, basal ganglia, thalamus, and back to motor cortex). Instead, the system consists of multiple segregated pathways, involving the entire frontal cortex, drawing on parallel processing to permit the planning, execution, and co-ordination of eye and limb movements and, by inference, other frontal lobe processes including those of the ‘limbic system’.

Tom Sears


See also brain; dopamine; grey matter; limbic system; movement, control of.

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basal ganglia

basal ganglia pl. n. several large masses of grey matter embedded deep within the white matter of the cerebrum. They include the caudate and lenticular nuclei (together known as the corpus striatum) and the amygdaloid nucleus. The lenticular nucleus consists of the putamen and globus pallidus. The basal ganglia are involved with the regulation of voluntary movements at a subconscious level.

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basal ganglia

basal ganglia Small masses of nervous tissue within the brain that connect the cerebrum with other parts of the nervous system. They are involved with the subconscious regulation of voluntary movements. The largest of the basal ganglia is the corpus striatum.

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Basal Ganglia

Basal Ganglia

The basal ganglia are subcortical nuclei that are highly developed in primates and are strongly interconnected with the neocortex. They are major components of the telencephalon (endbrain) in mammals and lie beneath the cerebral cortex, which forms the outer sheet of the endbrain. The basal ganglia include two well-known parts of the extrapyramidal motor system (the striatum and the pallidum). Technically, the amygdala is also part of the basal ganglia, but, as a functional system quite different from the striatopallidal complex, falls outside the scope of this article.

The basal ganglia are involved in motor and psychomotor control and are therefore a central focus for studies of Parkinson's disease and Huntington's disease, motor disorders involving reduced movement capacity (Parkinson's disease) or too much movement (Huntington's disease). It is recognized that the basal ganglia can affect neuropsychiatric and cognitive functions and that basal ganglia dysfunction thus may contribute to neuropsychiatric disorders. Examples of neuropsychiatric disorders involving the basal ganglia include obsessive-compulsive disorder and Tourette's syndrome.

The basal ganglia are part of cortico-basal ganglia circuits receiving inputs from the neocortex (and thalamus), processing that information, interacting with modulatory loop-circuits, and passing the processed information on to the frontal neocortex (via the thalamus) and to brainstem targets such as the superior colliculus and the reticular formation (see Figure 1). Nearly the entire cortex projects to the striatum, which is considered the main input site of the basal ganglia. The striatum, in turn, projects to the pallidum (globus pallidus), which gives rise to the main basal ganglia outflow to the thalamus and other sites. A remarkable characteristic of these basal ganglia connections is that they are inhibitory. The striatum inhibits the pallidum, and the pallidum inhibits the thalamus. This means that activation of the striatum can release the thalamus and other output targets (see Figure 1).

This double-inhibition circuit is considered to be critical to the release of movements and complex actions, probably including cognitive actions. An important aspect of the circuit is that most of the striatal neurons that project to the pallidum (projection neurons) fire action potentials phasically at low rates. But pallidal neurons fire tonically (nearly continuously) at high rates. These physiological findings suggest that the basal ganglia tonically inhibit their targets (e.g., the thalamus) but that when the striatum becomes active, this tonic inhibition is briefly (phasically) released. Because the inputs to the striatum are excitatory, the general circuit plan involves cortical excitation of the striatum, leading through the double inhibition to release of the thalamus. This release from inhibition (known as disinhibition) is considered to underlie the movement release-inhibition functions of the basal ganglia.

The striatum and pallidum act in close cooperation with two other nuclei, the substantia nigra and the subthalamic nucleus. The substantia nigra lies in the midbrain and attains a very large size in the human brain. The substantia nigra has two parts, one of which is called the pars reticulata and is very much like the pallidum. The nigral pars reticulata is, judging by its anatomy, likely to be a differentiated extra part of the pallidum displaced caudally into the mid-brain. Like the pallidum, the pars reticulata of the substantia nigra receives input from the striatum and projects strongly to the thalamus. An important difference from the pallidum is that the nigral pars reticulata also projects to the superior colliculus, a structure involved in controlling eye movements (especially saccadic eye movements). The second part of the substantia nigra is the pars compacta. Its neurons synthesize the neurotransmitter dopamine, and they give rise to the dopamine-containing nigrostriatal tract, which innervates the striatum and releases dopamine there. In Parkinson's disease, these neurons degenerate, leading to a loss of dopamine in the striatum.

The second nucleus closely associated with the striatum and pallidum is the subthalamic nucleus. This nucleus (named for the fact that it lies in the territory underneath the thalamus) is a key regulator of the release-inhibition functions of the basal ganglia (see Figure 2). It receives inhibitory input from the pallidum's so-called external segment and sends excitatory output back to the pallidum. It thus is disinhibited when the striatum is phasically activated, and it excites the pallidum's internal segment. This subthalamic loop or indirect pathway opposes the action of the direct pathway from striatum to internal pallidum to thalamus (see Figure 2).

The striatum, as the input side of the basal ganglia and as the first stage of the main pathways leading out from the basal ganglia, sets up important functional subdivisions of the basal ganglia and its circuits. The striatum has three anatomical subdivisions that roughly correspond to functional parts: the caudate nucleus, the putamen, and the ventral striatum. The caudate nucleus makes up the largest part of the striatum at anterior levels and receives strong inputs from the frontal cortex and some other areas of association cortex. The putamen is the large, laterally placed nucleus of the striatum and receives most of the input from sensorimotor and association cortex. The ventral striatum—which, as its name implies, lies at the base of the striatum—receives inputs related to the limbic system (including inputs from the hippocampal formation and amygdala).

All three of these large subdivisions of the striatum project to corresponding parts of the pallidum and substantia nigra. There is considerable evidence that these pathways are fairly distinct from one another, so that the functional channels set up in the striatum are maintained in the pallidum and substantia nigra and, in their outflow pathways, to the rest of the brain. This is true also for the dopamine-containing projections from the midbrain to the striatum. For example, medial to the nigra substantia pars compacta, in and near the midline of the midbrain, there are other dopamine-containing neurons that form the ventral tegmental area. This region innervates the ventral striatum and is part of reward circuits of the brain, mediating reward-based behaviors and some forms of drug addiction (e.g., to cocaine and amphetamine).

These functional subdivisions are differentially affected in the major disorders associated with basal ganglia dysfunction. The dorsal striatum (caudate nucleus and putamen) are abnormal in Parkinson's disease and Huntington's disease. The most severe motor disturbances in these disorders are associated with loss of dopamine (Parkinson's disease) or neurons (Huntington's disease) in the putamen, which receives inputs from sensory and motor cortex. Cognitive-affective disturbances in these disorders are associated with loss of function in the caudate nucleus, which receives inputs from frontal areas of the association cortex. Neuropsychiatric disorders ranging from obsessive-compulsive disorder to depression are also associated with abnormal function of the caudate nucleus. Dysfunction of the ventral striatum is suspected in some psychiatric disorders, including schizophrenia. The ventral tegmental area, which projects to the ventral striatum, is largely spared in Parkinson's disease. The anatomical organization of basal-ganglia pathways suggests that the cortically directed outflow of the basal ganglia mainly targets executive areas of the neocortex, including motor, premotor, or prefrontal cortex. The breadth of frontal cortex affected may also help to account for the broad functional influences of the basal ganglia suggested by clinical evidence.

Some disorders affecting the basal ganglia are associated with major changes in neurotransmitter systems in basal-ganglia circuits. Drugs affecting these systems include not only levodopa, given to Parkinson's patients as a replacement therapy for the lost dopamine, but also agents with powerful effects on mental activity and behavior, including antipsychotics such as haloperidol (a dopamine receptor antagonist) and psychoactive drugs such as marijuana. This large range also conforms to evidence that the basal ganglia mediate cognitive-affective as well as motor functions.

The basal ganglia are implicated not only in the continuing control of action but also in the learning mechanisms that underlie the development of the near-automatic behaviors that we think of as habits and rituals. Studies of these learning functions of the basal ganglia suggest that the anatomical circuits summarized here are actually highly dynamic networks. Recordings from behaving animals suggest that the activity patterns of neurons in the striatum undergo major changes as the animals become conditioned or learn new procedures. A teaching signal for the striatal neurons is thought to come from the dopamine-containing neurons of the substantia nigra. This new evidence suggests that the very nuclei disabled in disorders such as Parkinson's disease and Huntington's disease normally help to modify cortico-basal ganglia circuits as a result of experience, so that habits and procedures can be learned and produced as whole sequences or chunks. Such automatized behaviors are fundamentally important in freeing the brain to react to new events in the environment and to carry out many cognitive functions. The basal ganglia, then, may provide a base for cognitive activity as well as for motor activity.

See also:REINFORCEMENT OR REWARD IN LEARNING: ANATOMICAL SUBSTRATES; REINFORCEMENT OR REWARD IN LEARNING: STRIATUM

Bibliography

Graybiel. A. M. (1997). The basal ganglia and cognitive pattern generators. Schizophrenia Bulletin 23, 459-469.

Graybiel, A. M., Aosaki, T., Flaherty, A. W., and Kimura, M. (1994). The basal ganglia and adaptive motor control. Science 265, 1,826-1,831.

Graybiel A. M., and Penney J. B. (1999). Chemical architecture of the basal ganglia. In F. E. Bloom, A. Björklund, and T. Hökfelt, eds., Handbook of chemical neuroanatomy. Amsterdam: Elsevier.

Graybiel, A. M., and Rauch, S. L. (2000). Toward a neurobiology of obsessive-compulsive disorder. Neuron 28, 343-347.

Hikosaka O., Miyashita K., Miyachi S., Sakai K., and Lu, X. (1998). Differential roles of the frontal cortex, basal ganglia, and cerebellum in visuomotor sequence learning. Neurobiology of Learning and Memory 70 137-149.

Leckman, J. F., and Riddle, M. A. (2000). Tourette's syndrome: When habit-forming systems form habits of their own? Neuron 28, 349-354.

Mink, J. W. (1996). The basal ganglia: Focused selection and inhibition of competing motor programs. Progressive Neurobiology 50, 381-425.

Salmon, D. P., and Butters, N. (1995). Neurobiology of skill and habit learning. Current Opinion in Neurobiology 5, 184-190.

White, N. M. (1997). Mnemonic functions of the basal ganglia. Current Opinion in Neurobiology 7, 164-169.

Wichmann T., and DeLong, M. R. (1996). Functional and pathophysiological models of the basal ganglia. Current Opinion in Neurobiology 6, 751-758.

Ann M.Graybiel

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