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Basal ganglia comprises several subcortical nuclei which have different neurochemical and physiological characteristics. This article reviews the actual knowledge about the anatomy and physiology of the basal ganglia as well as its role in motor control.
Basal ganglia have been known as a motor center because their lesions cause motor disturbances in involuntary movements such as chorea, ballism or akinesia in Parkinsonism. The different types of involuntary movements are closely related to the underlying muscle tone. Mechanisms of bradykinesia or akinesia have been elaborated in physiological studies on Parkinson's disease, and the significance of sensorimotor processing or attention, arousal has been disclosed as a relevant factor of bradykinesia. Cognitive functions of the basal ganglia have attracted attention, particularly in the disorder of Parkinson's disease. Subcortical dementia, difficulty in formation or changes of concepts, is encountered in advanced stages of Parkinson's disease. Whether cognitive functions in the frontostriatal system are primarily related to the motor function of the brain is an issue for future study.
Basal ganglia have been known as a motor center because their lesions cause motor disturbances in involuntary movements such as chorea, ballism or akinesia in parkinsonism. The different types of involuntary movements are closely related to the underlying muscle tone. Mechanisms of bradykinesia or akinesia have been elaborated in physiological studies on Parkinson's disease and the significance of sensorimotor processing or attention arousal has been disclosed as a relevant factor of bradykinesia. Analysis of short-stepped gait, frozen gait or apraxia of gait, has claimed the frontal lobe and the striatum to be a locomotion center especially in humans (bipedal locomotion). Cognitive function of the basal ganglia has attracted attention particularly in the disorder of Parkinson's disease. Subcortical dementia, difficulty in formation or changes of concepts are encountered in advanced stages of Parkinson's disease. Whether cognitive functions in the frontostriatal system are primarily related to the motor function of the brain is an issue for future study.
Histochemical, pathway tracing, and neuropeptide/neurotransmitter localization studies in birds, reptiles and mammals during the 1970s and 80s clearly showed that the telencephalon in all amniotes consists of a prominent ventrally situated subpallial region termed the basal ganglia, and a large overlying region involved in higher order information processing termed the pallium or cortex. These studies also showed that the basal ganglia in all extant amniote groups possessed neurochemically and hodologically distinct striatal and pallidal territories. More recently, studies of the localization of genes controlling regional brain development have confirmed the homology of the basal ganglia among amniotes. In our ongoing studies, we have identified several aspects of the functional organization of the basal ganglia that birds also share with mammals. These include: (1) an extensive glutamatergic "cortico"-striatal input and distinctive, cell-type specific localization of glutamate receptor subtypes; (2) an extensive, presumptively glutamatergic intralaminar thalamic input to striatal neurons; (3) an extensive dopaminergic input from the midbrain targeting both substance P (SP) type and enkephalin (ENK) type striatal projection neurons, with SP-type striatal neurons seemingly richer in the D-1 type dopamine receptor; and (4) SP+ and ENK+ striatal outputs giving rise to functionally distinct so-called direct and indirect motor output pathways, with the direct pathway having a pallido-thalamo-motor cortex loop and the indirect pathway relaying back to the direct circuit via the subthalamic nucleus. These findings suggest that the major aspects of the cellular organization and functional circuitry of the basal ganglia in stem amniotes were already as observed in living amniotes, as therefore presumably was its key role in movement control. Because the organization of the basal ganglia of anamniotes is clearly less elaborate than in amniotes, and because the basal ganglia and cortex in amniotes are clearly extensively interconnected structures, it seems likely that stem amniotes were characterized by a major step forward in the grade of telencephalic organization of both the basal ganglia and the pallium.
The basal ganglia in modern mammals, birds and reptiles (i.e. modern amniotes) are very similar in connections and neurotransmitters, suggesting that the evolution of the basal ganglia in amniotes has been very conservative. For example, the basal ganglia in all amniotes possess a dorsal striatum containing two main populations of projection neurons, substance P-containing (SP+) and enkephalin-containing (ENK+) neurons, which have major projections to the dorsal pallidum and the tegmentum (ventral tegmental area and substantia nigra, or VTA/SN). The VTA/SN, in turn, has a major dopaminergic (DA+) projection to the striatum in all amniotes. In this paper, we review these data on the basal ganglia in amniotes and note points of similarity and difference in the functional circuitry of the basal ganglia among amniotes. In addition, we review recent findings on the neurotransmitter organization and connectivity of the basal ganglia in amphibians and fishes, with the goal of assessing whether a basal ganglia showing the same basic features as in amniotes is observed in anamniotes. Published data indicate that in at least two groups of fishes (cartilaginous fishes and lungfishes) and apparently in amphibians, the basal ganglia is present and consists of a distinct striatum and pallidum. The striatum of amphibians, cartilaginous fishes, and lungfishes contain SP+ and ENK+ neurons that seem to project to the pallidum as well as to a brainstem cell group that appears comparable to the VTA/SN of amniotes. Data for ray-finned fishes also suggest the presence of a striatum containing SP+ and ENK+ neurons that projects to VTA/SN-like brainstem cell group. In the basal ganglia of ray-finned fishes, however, a distinct pallidum had not been identified. Finally, the brainstem cell group receiving striatal input in all anamniotes contains DA+ neurons that seem to project to the striatum. The present analysis suggests that a rudimentary basal ganglia was already present in the brain of the ancestral jawed vertebrates. This rudimentary basal ganglia likely consisted of a striatum and a pallidum, and the striatum probably already possessed the same basic connections and some of the same basic cell types as the basal ganglia of modern jawed vertebrates.
The ascending cholinergic projections of the pedunculopontine and dorsolateral tegmental nuclei, referred to collectively as the pontomesencephalotegmental (PMT) cholinergic complex, were investigated by use of fluorescent tracer histology in combination with choline-O-acetyltransferase (ChAT) immunohistochemistry and acetylcholinesterase (AChE) pharmacohistochemistry. Propidium iodide, true blue, or Evans blue was infused into the anterior, reticular, mediodorsal, central medial, and posterior nuclear areas of the thalamus; the habenula; lateral geniculate; superior colliculus; pretectal/parafascicular area; subthalamic nucleus; caudate-putamen complex; globus pallidus; entopeduncular nucleus; substantia nigra; medial septal nucleus/vertical limb of the diagonal band area; magnocellular preoptic/ventral pallidal area; and lateral hypothalamus. In some animals, separate injections of propidium iodide and true blue were made into two different regions in the same rat brain, usually a dorsal and a ventral target, in order to assess collateralization patterns. Retrogradely transported fluorescent labels and ChAT and/or AChE were analyzed microscopically on the same brain section. All of the above-delimited targets were found to receive cholinergic input from the PMT cholinergic complex, but some regions were preferentially innervated by either the pedunculopontine or dorsolateral tegmental nucleus. The former subdivision of the PMT cholinergic complex projected selectively to extrapyramidal structures and the superior colliculus, whereas the dorsolateral tegmental nucleus was observed to provide cholinergic input preferentially to anterior thalamic regions and rostral portions of the basal forebrain. The PMT cholinergic neurons showed a tendency to collateralize extensively.
A-type K(+) currents are key determinants of repetitive activity and synaptic integration. Although several gene families have been shown to code for A-type channel subunits, recent studies have suggested that Kv4 family channels are the principal contributors to A-type channels in the somatodendritic membrane of mammalian brain neurons. If this hypothesis is correct, there should be a strong correlation between Kv4 family mRNA and A-type channel protein or aggregate channel currents. To test this hypothesis, quantitative single-cell reverse transcription-PCR analysis of Kv4 family mRNA was combined with voltage-clamp analysis of A-type K(+) currents in acutely isolated neurons. These studies revealed that Kv4.2 mRNA abundance was linearly related to A-type K(+) current amplitude in neostriatal medium spiny neurons and cholinergic interneurons, in globus pallidus neurons, and in basal forebrain cholinergic neurons. In contrast, there was not a significant correlation between estimates of Kv4.1 or Kv4.3 mRNA abundance and A-type K(+) current amplitudes. These results argue that Kv4.2 subunits are major constituents of somatodendritic A-type K(+) channels in these four types of neuron. In spite of this common structural feature, there were significant differences in the voltage dependence and kinetics of A-type currents in the cell types studied, suggesting that other determinants may create important functional differences between A-type K(+) currents.
The basal ganglia are composed of a set of forebrain structures implicated in the adaptive control of behaviour. These structures process information originating from the entire cerebral cortex, as well as from nonspecific thalamic nuclei and the amygdala. In turn, they redistribute the integrated signals toward thalamic and brainstem nuclei related to motor, premotor, prefrontal and limbic cortical areas. During the two last decades, there has been increasing experimental evidence that the basal ganglia circuitry may be part of a remote control system influencing the spread of epileptic seizures. In the present article, we review the basic principles of the functional organization of the basal ganglia and provide experimental data on the activity that is transmitted by the cerebral cortex to the input stage of the basal ganglia during absence seizures. The functional organization of the basal ganglia supports the current hypothesis that these structures can dynamically control generalized seizures through their input-output relationships.
The basal ganglia are a group of subcortical nuclei involved in a variety of processes including motor, cognitive and mnemonic functions. One of their major roles is to integrate sensorimotor, associative and limbic information in the production of context-dependent behaviours. These roles are exemplified by the clinical manifestations of neurological disorders of the basal ganglia. Recent advances in many fields, including pharmacology, anatomy, physiology and pathophysiology have provided converging data that have led to unifying hypotheses concerning the functional organisation of the basal ganglia in health and disease. The major input to the basal ganglia is derived from the cerebral cortex. Virtually the whole of the cortical mantle projects in a topographic manner onto the striatum, this cortical information is 'processed' within the striatum and passed via the so-called direct and indirect pathways to the output nuclei of the basal ganglia, the internal segment of the globus pallidus and the substantia nigra pars reticulata. The basal ganglia influence behaviour by the projections of these output nuclei to the thalamus and thence back to the cortex, or to subcortical 'premotor' regions. Recent studies have demonstrated that the organisation of these pathways is more complex than previously suggested. Thus the cortical input to the basal ganglia, in addition to innervating the spiny projection neurons, also innervates GABA interneurons, which in turn provide a feed-forward inhibition of the spiny output neurons. Individual neurons of the globus pallidus innervate basal ganglia output nuclei as well as the subthalamic nucleus and substantia nigra pars compacta. About one quarter of them also innervate the striatum and are in a position to control the output of the striatum powerfully as they preferentially contact GABA interneurons. Neurons of the pallidal complex also provide an anatomical substrate, within the basal ganglia, for the synaptic integration of functionally diverse information derived from the cortex. It is concluded that the essential concept of the direct and indirect pathways of information flow through the basal ganglia remains intact but that the role of the indirect pathway is more complex than previously suggested and that neurons of the globus pallidus are in a position to control the activity of virtually the whole of the basal ganglia.
The basal ganglia are known to receive inputs from widespread regions of the cerebral cortex, such as the frontal, parietal, and temporal lobes. Of these cortical areas, only the frontal lobe is thought to be the target of basal ganglia output. One of the cortical regions that is a source of input to the basal ganglia is area TE, in inferotemporal cortex. This cortical area is thought to be critically involved in the recognition and discrimination of visual objects. Using retrograde transneuronal transport of herpes simplex virus type 1, we have found that one of the output nuclei of the basal ganglia, the substantia nigra pars reticulata, projects via the thalamus to TE. Thus, TE is not only a source of input to the basal ganglia, but also is a target of basal ganglia output. This result implies that the output of the basal ganglia influences higher order aspects of visual processing. In addition, we propose that dysfunction of the basal ganglia loop with TE leads to alterations in visual perception, including visual hallucinations.
Basal ganglia disorders are a heterogeneous group of clinical syndromes with a common anatomic locus within the basal ganglia. To account for the variety of clinical manifestations associated with insults to various parts of the basal ganglia we propose a model in which specific types of basal ganglia disorders are associated with changes in the function of subpopulations of striatal projection neurons. This model is based on a synthesis of experimental animal and post-mortem human anatomic and neurochemical data. Hyperkinetic disorders, which are characterized by an excess of abnormal movements, are postulated to result from the selective impairment of striatal neurons projecting to the lateral globus pallidus. Hypokinetic disorders, such as Parkinson's disease, are hypothesized to result from a complex series of changes in the activity of striatal projection neuron subpopulations resulting in an increase in basal ganglia output. This model suggests that the activity of subpopulations of striatal projection neurons is differentially regulated by striatal afferents and that different striatal projection neuron subpopulations may mediate different aspects of motor control.
There has been a growing interest in the differential role of various neural structures in implicit learning processes. The goal of our study was to clarify how focal lesions restricted to the basal ganglia interfere with different aspects of implicit visuo-motor sequence learning. A version of the Serial Reaction Time Task (SRTT) of Nissen and Bullemer using a 12-trial sequence was administered. A total of 20 subjects with focal basal ganglia lesions caused by ischemic or hemorrhagic infarction and 20 matched control subjects participated in this study. The results indicate that subjects with focal basal ganglia lesions showed unimpaired implicit learning of a 12-item motor sequence. Subjects with basal ganglia lesions, however, had more difficulties improving their general proficiency with the reaction-time task independent of sequence-specific learning. We observed a tendency toward smaller regional volumes in the cerebellum and left pre-supplementary motor area (pre-SMA) of subjects with basal ganglia lesions. Smaller cerebellar and pre-SMA volumes were related to lower implicit learning performance in the lesion group. The size of lesions in the basal ganglia was not related to sequence-specific implicit learning but had a significant influence on subjects' general proficiency for execution of the reaction-time task. We propose that implicit learning is achieved by a distributed network of cortical and subcortical structures. The basal ganglia seem to be responsible for adjusting to the general requirements of a task rather than for learning specific associations between stimuli that might be accomplished by premotor frontal areas and the cerebellum instead.
The basal ganglia consist of five interconnected nuclei in the basal forebrain that influence cortical control of voluntary movement. Synaptic information travels through the basal ganglia using distinct pathways from the input structure, the striatum, to the output nuclei, the substantia nigra pars reticulata and the globus pallidus internal segment. The activity of the striatal output pathways is influenced by glutamatergic input from the cerebral cortex, dopaminergic input from the substantia nigra pars compacta, and cholinergic interneurons. Since the basal ganglia output nuclei tonically inhibit the motor nuclei of the thalamus, the basal ganglia facilitate motor activity by disinhibiting the thalamus.
Previous immunohistochemical studies have provided evidence that the external segment of the globus pallidus extends ventrally beneath the transverse limb of the anterior commissure into the area of the substantia innominata. Enkephalin-positive staining in the form of "woolly fibers" has been used as a marker for the globus pallidus and its ventral extension. Acetylcholinesterase staining of both fibers and cell bodies, frequently used as a marker for the basal nucleus of Meynert, is also found in the area of the substantia innominata. This study describes the differential distribution of enkephalin-positive woolly fibers and acetylcholinesterase staining on adjacent sections in both the monkey and human basal forebrain area in an attempt to define the relationship between the basal ganglia and the basal nucleus of Meynert. The results show that while both occupy large regions of the basal forebrain, they overlap very little. In both species investigated, dense concentrations of acetylcholinesterase-positive neurons lie, for the most part, outside the boundaries of the pallidal fibers. However, some scattered acetylcholinesterase cells do lie within the confines of the dorsal pallidum, and a more prominent group is found in the subcommissural ventral pallidum. These cells may constitute a group separate from the more densely packed acetylcholinesterase-positive cells in woolly fiber-free regions in that they may receive direct striatal input.
The basal ganglia consist of several interconnected nuclei located in the telecephalon, diencephalon and mesencephalon that are involved in a variety of motor and non-motor behavioural functions. Glutamate receptors play a major role in neurotransmission within the basal ganglia and are present in all nuclei of the basal ganglia. This review focuses on the contribution of the NMDA class of glutamatergic receptors to various movement disorders whose primary pathology lies within the basal ganglia and discusses how pharmacological manipulation of such receptors may be therapeutically useful.
Basal ganglia calcification (BGC) is now being diagnosed with increasing frequency with widespread application of computed tomography (CT) in clinical practice and is no more considered a rarity. During the period 1987 to 1995, 42 patients were noted to have BGC and it constituted 0.93% of all CT scan of brain carried out during the relevant period. These patients presented with diverse neurological and endocrine disorders i.e., epilepsy (22 patients), mental retardation (five patients), extra-pyramidal syndromes (five patients), abnormal behaviour (three patients), stroke (two patients), raised intracranial tension without localizing signs (one patient), following radiotherapy (one patient), and with hypoparathyroidism (three patients). These patients were noted to have variable degree of calcification in different parts of brain i.e., basal ganglia (42 cases), cerebellum (12 cases) and cerebral cortex (nine cases). Family history of a neurological disorder was available in five patients. This study highlights the fact that calcification of basal ganglia and other parts of the brain is often a nonspecific finding on CT scan and it may not be possible to establish a clinicopathological correlation.
The subthalamic nucleus and the external pallidum (GPe) are classically viewed as part of the so-called indirect pathway, which acts in concert with the direct pathway. The direct and indirect pathways form the conceptual framework of the anatomical and functional organization of the basal ganglia. A review of recent data regarding the connections of the subthalamic nucleus and the GPe has revealed a lack of firm anatomical support for the existence of the indirect pathway. However, newly recognized projections of the subthalamic nucleus and the GPe place these structures on various novel routes that change the conceptual architecture of the basal ganglia circuitry. These new findings force us to modify our view of the functional identity of the subthalamic nucleus and the GPe. In this new perspective, the GPe stands as an additional integrative station, together with the striatum and the internal pallidum and substantia nigra pars reticulata (GPi/SNr), along the main steam of information processing within the basal ganglia circuitry. Because of its crucial position between the input and output stations of the basal ganglia, the GPe can markedly influence the neuronal computation that occurs at GPi/SNr levels. The subthalamic nucleus can still be regarded as a 'control structure' lying alongside the main stream of information processing. However, because of its widespread efferent projections, the subthalamic nucleus exerts its driving effect on most components of the basal ganglia. Its action is mediated not only by the indirect pathway, but by a multitude of mono- and polysynaptic projections that ultimately reach the basal ganglia output cells.
Germ-cell tumors of the central nervous system generally develop in the midline, but the tumors can also occur in the basal ganglia and/or thalamus. However, MR images have rarely been documented in the early stage of the tumor in these regions. We retrospectively reviewed MR images obtained on admission and approximately 3 years earlier in two patients with germinoma in the basal ganglia, and compared them with CT. In addition to hyperdensity on CT, both hyperintensity on T1-weighted images and a small hyperintense lesion on T2-weighted images were commonly seen in the basal ganglia. These findings may be early MRI signs of germinoma in this region, and the earliest and most characteristic diagnostic feature on MRI was atrophy of the basal ganglia, which was recognizable before development of hemiparesis.