CHAPTER 22 Basal ganglia

The term basal ganglia is used to denote a number of subcortical nuclear masses that lie in the inferior part of the cerebral hemisphere, in close relation with the internal capsule (Figs 22.1, 22.2; see Fig. 23.28). The traditional definition of the basal ganglia included the corpus striatum, claustrum, and amygdaloid complex. The term has now been restricted to the corpus striatum and its associated structures in the diencephalon and midbrain; collectively they form a functional complex involved in the control of movement and motivational aspects of behaviour. The function of the claustrum is unknown; the amygdala is more closely related to the limbic system and is therefore described in that context (see Ch. 23).

Fig. 22.1 Axial (A) and coronal (B) MR images of the brain.

Fig. 22.2 Oblique coronal section of the brain.

(Dissection by EL Rees; photograph by Kevin Fitzpatrick on behalf of GKT School of Medicine, London.)

The corpus striatum consists of the caudate nucleus, putamen and globus pallidus (Fig. 22.3). Because of their close proximity, the putamen and globus pallidus were once considered as an entity, termed the lentiform (lenticular) complex or nucleus. However, although the name has been retained in gross anatomical terminology and in some compound names (e.g. sublenticular, retrolenticular), it is now known that the putamen and caudate nucleus share a common chemocytoarchitecture and connections, and they are referred to jointly as the neostriatum or simply the striatum.

Fig. 22.3 Terminology and relationships of structures forming the basal ganglia.

The striatum is considered to be the principal ‘input’ structure of the basal ganglia since it receives the majority of afferents from other parts of the neuraxis. Its principal efferent connections are to the globus pallidus and pars reticulata of the substantia nigra. The globus pallidus and, more particularly, its medial segment, together with the pars reticulata of the substantia nigra is regarded as the main ‘output’ structure because it is the source of basal ganglia efferent fibre projections, mostly directed to the thalamus.

Disorders of the basal ganglia are principally characterized by abnormalities of movement, muscle tone and posture. There is a wide spectrum of clinical presentations ranging from poverty of movement and hypertonia at one extreme (typified by Parkinson’s disease) to abnormal involuntary movements (dyskinesias) at the other. The underlying pathophysiological mechanisms that mediate these disorders have been much studied in recent years and are better understood than for any other type of complex neurological dysfunction. This has led to the introduction of new rational therapeutic strategies for both medical and neurosurgical treatment of movement disorders.

The caudate nucleus is a curved, tadpole-shaped mass. It has a large anterior head, which tapers to a body, and a down-curving tail (Fig. 22.4). The head is covered with ependyma and lies in the floor and lateral wall of the anterior horn of the lateral ventricle, in front of the interventricular foramen. The tapering body is in the floor of the body of the ventricle, and the narrow tail follows the curve of the inferior horn, and so lies in the ventricular roof, in the temporal lobe. Medially, the greater part of the caudate nucleus abuts the thalamus, along a junction that is marked by a groove, the sulcus terminalis. The sulcus contains the stria terminalis, lying deep to the ependyma (Fig. 22.5). The sulcus terminalis is especially prominent anterosuperiorly (because of the large size of the head and body of the caudate nucleus relative to the tail), and here the stria terminalis is accompanied by the thalamostriate vein.

Fig. 22.4 The striatum within the left cerebral hemisphere.

(By permission from Crossman AR, Neary D 2000 Neuroanatomy, 3rd edn. Edinburgh: Churchill Livingstone.)

Fig. 22.5 An oblique section through the diencephalon and basal ganglia. ICV, internal cerebral veins; H, H₁, H₂, subthalamic fields of Forel.

The corpus callosum lies above the head and body of the caudate nucleus. The two are separated laterally by the fronto-occipital fasciculus, and medially by the subcallosal fasciculus which caps the nucleus (Figs 22.5, 22.6). The caudate nucleus is largely separated from the lentiform complex by the anterior limb of the internal capsule (Figs 22.1, 22.6 and 22.7). However, the inferior part of the head of the caudate becomes continuous with the most inferior part of the putamen immediately above the anterior perforated substance; this junctional region is sometimes known as the fundus striati (Fig. 22.6). Variable bridges of cells connect the putamen to the caudate nucleus for most of its length. They are most prominent anteriorly, in the region of the fundus striati and the head and body of the caudate nucleus, where they break up the anterior limb of the internal capsule (Fig. 22.7). In the temporal lobe, the anterior part of the tail of the caudate nucleus becomes continuous with the posteroinferior part of the putamen. The vast bulk of the caudate nucleus and putamen are often referred to as the dorsal striatum. A smaller inferomedial part of the rostral striatum is referred to as the ventral striatum, and includes the nucleus accumbens.

Fig. 22.6 Coronal sections through the corpus striatum and anterior perforated substance. A is anterior to B.

Fig. 22.7 Posterior aspect of a coronal section through the anterior horn of the lateral ventricles.

The lentiform complex (Figs 22.1, 22.2, 22.8) lies deep to the insular cortex, with which it is roughly coextensive, although they are separated by a thin layer of white matter and by the claustrum. The latter splits the insular subcortical white matter to create the extreme and external capsules; the external capsule separates the claustrum from the putamen. The internal capsule separates the lentiform complex from the caudate nucleus.

Fig. 22.8 Anterior aspect of a coronal section through the left cerebral hemisphere.

The lentiform complex consists of the laterally placed putamen and the more medial globus pallidus (pallidum), which are separated by a thin layer of fibres, the lateral or external medullary lamina. The globus pallidus is itself divided into two segments, a lateral (or external) segment and a medial (or internal) segment, separated by an internal (or medial) medullary lamina. The two segments have distinct afferent and efferent connections.

Inferiorly, a little behind the fundus striati, the lentiform complex is grooved by the anterior commissure, which connects inferior parts of the temporal lobes and the anterior olfactory cortex of the two sides (Fig. 22.6). The area above the commissure is referred to as the dorsal pallidum, and that below it as the ventral pallidum.

STRIATUM

The striatum consists of the caudate nucleus, putamen and ventral striatum, which are all highly cellular and well vascularized. The caudate and putamen are traversed by numerous small bundles of thinly-myelinated, or non-myelinated, small-diameter axons, which are mostly striatal afferents and efferents. They radiate through the striatal tissue as though converging on, or radiating from, the globus pallidus. The bundles are occasionally referred to by the archaic term ‘Wilson’s pencils’ and they account for the striated appearance of the corpus striatum.

Neurones of both dorsal and ventral striatum are mainly medium-sized multipolar cells. They have round, triangular or fusiform somata, mixed with a smaller number of large multipolar cells. The ratio of medium to large cells is at least 20 : 1. The large neurones have extensive spherical or ovoid dendritic trees up to 60 μm across. The medium-sized neurones also have spherical dendritic trees, approximately 20 μm across, which receive the synaptic terminals of many striatal afferents. The dendrites of both medium and large striatal cells may be either spiny or non-spiny. The most common neurone (usually 75% of the total) is a medium-sized cell with spiny dendrites. These cells utilize γ-aminobutyric acid (GABA) as their transmitter and also express the genes coding for either enkephalin or substance P/dynorphin. Enkephalinergic neurones express D2 dopamine receptors. Substance P/dynorphin neurones express D1 receptors. These neurones are the major, and perhaps exclusive, source of striatal efferents to the pallidum and substantia nigra pars reticulata. The remaining medium-sized striatal neurones are aspiny, and are intrinsic cells that contain acetylcholinesterase (AChE), choline acetyltransferase (CAT) and somatostatin. Large neurones with spiny dendrites contain AChE and CAT; most, perhaps all, are intrinsic neurones. Aspiny large neurones are all intrinsic neurones.

Intrinsic synapses are probably largely asymmetric (type II), while those derived from external sources are symmetric (type I). The aminergic afferents from the substantia nigra, raphe and locus coeruleus all end as profusely branching axons with varicosities, which contain dense-core vesicles (the presumed store of amine transmitters). Many of these varicosities have no conventional synaptic membrane specializations, and may release transmitter in a way analogous to that found in peripheral postsynaptic sympathetic axons.

Neuroactive chemicals, whether intrinsic or derived from afferents, are not distributed uniformly in the striatum. For example, serotonin and glutamic acid decarboxylase (GAD) concentrations are highest caudally, while substance P, acetylcholine (ACh) and dopamine are highest rostrally. However, there is a finer grain neurochemical organization that informs the view of the striatum as a mosaic of islands or striosomes (sometimes referred to as patches), each 0.5–1.5 mm across, packed into a background matrix. Striosomes contain substance P and enkephalin. During development, the first dopamine terminals from the substantia nigra are found in striosomes. Although this exclusivity does not persist after birth, striosomes in the adult caudate nucleus still contain a higher concentration of dopamine than the matrix. The latter contains ACh and somatostatin and is the target of thalamostriate axons. Receptors for at least some neurotransmitters are also differentially distributed. For example, opiate receptors are found almost exclusively within striosomes, and muscarinic receptors predominantly so. Moreover, the distribution of neuroactive substances within the striosomes is not uniform. In humans, the striosome/matrix patchwork is less evident in the putamen, where it appears to consist predominantly of matrix, than it is in the caudate nucleus.

All afferents to the striatum terminate in a mosaic manner. The size of a cluster of terminals is usually 100–200 μm across. Some afferent terminal clusters are not arranged in register with the clear striosome/matrix distributions seen in nigrostriatal and thalamostriatal axons. In general, afferents from neocortex end in striatal matrix and those from allocortex end in striosomes. However, the distinction is not absolute: although afferents from the neocortex arise in layers V and VI, those from the superficial part of layer V end predominantly in striatal matrix, whereas those from deeper neocortex project to striosomes. Striatal cell bodies, which are the sources of efferents, also form clusters, but again are not uniformly related to striosomes. For example, the cell bodies of some striatopallidal and striatonigral axons lie clustered within striosomes, and others lie outside them, but still in clusters. The neurones and neuropil of the ventral striatum are essentially similar to those of the dorsal striatum, but the striosomal/matrix organization is less well-defined, and seems to consist predominantly of striosomes.

The major connections of the striatum are summarized in Fig. 22.9. Although the connections of the dorsal and ventral divisions overlap, the generalization can be made that the dorsal striatum is predominantly connected with motor and associative areas of the cerebral cortex, whilst the ventral striatum is connected with the limbic system and orbitofrontal and temporal cortices. For both dorsal and ventral striatum, the pallidum and substantia nigra pars reticulata are key efferent structures. The fundamental arrangement is the same for both divisions. The cerebral cortex projects to the striatum, which in turn projects to the pallidum and substantia nigra pars reticulata, and efferents from the pallidum and substantia nigra pars reticulata influence the cerebral cortex (either the supplementary motor area or prefrontal and cingulate cortices via the thalamus) and the superior colliculus (see below).