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Neuropsychiatry of the Basal Ganglia H a Ring, J Serra-Mestres

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Neuropsychiatry of the Basal Ganglia H a Ring, J Serra-Mestres Downloaded from http://jnnp.bmj.com/ on February 6, 2016 - Published by group.bmj.com 12 ADVANCES IN NEUROPSYCHIATRY Neuropsychiatry of the basal ganglia H A Ring, J Serra-Mestres ............................................................................................................................. J Neurol Neurosurg Psychiatry 2002;72:12–21 This review aims to relate recent findings describing the parts of the basal ganglia closest to limbic role and neural connectivity of the basal ganglia to the structures and that are involved in cognitive and behavioural functions. The term includes the clinical neuropsychiatry of basal ganglia movement nucleus accumbens.1 This structure can be di- disorders and to the role of basal ganglia disturbances vided into a central core surrounded on its medial in “psychiatric”’ states. Articles relating to the relevant and ventral sides by a shell. The core is generally similar to the rest of the caudate/putamen and it topics were initially collected through MEDLINE and is difficult to identify a distinct dorsal border papers relating to the clinical conditions discussed were between the core and the neighbouring striatum. also reviewed. The anatomy and connections of the The shell has a rich dopaminergic innervation arising from the ventral tegmental area and dense basal ganglia indicate that these structures are innervation from the basolateral complex of the important links between parts of the brain that have amygdala.2 classically been considered to be related to emotional Some authorities also include the amygdala within a consideration of the basal ganglia as it functioning and brain regions previously considered to occupies an important position between the basal have largely motor functions. The basal ganglia have a ganglia and the limbic system and may play a part role in the development and integration of psychomotor in integrating activity between these structures.3 Embryological evidence supports inclusion of the behaviours, involving motor functions, memory and amygdala. The basal ganglia develop as part of the attentional mechanisms, and reward processes. telencephalon, from the basal region of the man- .......................................................................... tle layer of the primitive telencephalic vesicle and the amygdala complex develops from the same tissue mass as the caudate nucleus.3 asal ganglia disorders are characterised by These findings emphasise that there are impor- the presence of abnormal movements, psy- tant links between parts of the brain that have Bchiatric signs and symptoms, and varying classically been considered to be related to degrees of cognitive impairment. Traditionally, emotional functioning and parts of the brain that more attention has been paid to the motor abnor- have in the past been considered to play a part malities in these conditions than to the mental largely in motor functions. state and cognitive disturbances, despite the fact that these can be as disabling and distressing for Connections of the basal ganglia both the patients and their carers as the abnormal The complex consequences of disturbances to the movements. However, in recent years there has basal ganglia may be better understood when the been increasing recognition of the non-motor connections of these structures are considered. consequences of disease of the basal ganglia. At The striatum is the major receptive component of the same time there have been major advances in the basal ganglia. It receives massive inputs from our understanding of the functional anatomy and much of the cerebral cortex, from the substantia physiology of the basal ganglia and associated nigra, and the lateral amygdala, among other brain regions. This article will review recent regions. Recent ideas regarding the connections developments in these fields, with particular ref- of the basal ganglia have been shaped by descrip- erence to information helpful in understanding tions of parallel circuits linking cortical associ- why basal ganglia diseases are so often associated ation areas, through basal ganglia and thalamus, with the development of psychiatric symptoms. back to cortex. WHAT ARE THE BASAL GANGLIA? Initially two loops were suggested, a motor loop See end of article for passing through the putamen and an association authors’ affiliations Anatomy of the basal ganglia The basal ganglia are large subcortical nuclear or complex “loop” passing through the caudate. ....................... 4 masses. The naming of the basal ganglia has led Subsequently Alexander et al, using the “motor” Correspondence to: to some confusion over the years as has the circuit as a model, described evidence for other Dr H Ring, Academic circuits. These circuits followed the general Department of Psychiatry, debate as to which structures should be included St Bartholomew’s and the within this description. It is agreed that core Royal London School of components comprise the caudate nucleus, the ................................................. Medicine, Whitechapel nucleus accumbens, the putamen, and the globus Road, London E1 1BB, UK pallidus. The caudate nucleus and putamen Abbreviations: PD, Parkinson’s disease; SSRIs, selective Received together are sometimes called the striatum, and serotonin re-uptake inhibitors; ECT, electroconvulsive 12 January 2001 the putamen and globus pallidus are together therapy; HD, Huntington’s disease; PSP, progressive In revised form 30 May supranuclear palsy; WD, Wilson’s disease; FD, Fahr’s 2001 sometimes described as the lentiform nucleus. disease; GTS, Gilles de la Tourette’s syndrome; OCD, Accepted 27 June 2001 More recently an additional term, “ventral obsessive-compulsive disorder; ADHD, attention deficit ....................... striatum” has been introduced to describe those disorder with hyperactivity www.jnnp.com Downloaded from http://jnnp.bmj.com/ on February 6, 2016 - Published by group.bmj.com Neuropsychiatry of the basal ganglia 13 principle that they were segregated from each other and that terms of clinical applications however, current employment of output from the circuits were transmitted to restricted existing knowledge relates largely to interactions between portions of the frontal lobe. These circuits, which have subse- dopamine and acetylcholine in Parkinson’s disease, and quently become well known and have formed the basis of fur- between dopamine and serotonin in modulating the motor ther investigation of basal ganglia function, were named as side effects of psychotropic medication.12 the “motor circuit”, the “occulomotor circuit”, the “dorsola- teral prefrontal circuit”, the “lateral orbitofrontal circuit” and Functions of the basal ganglia the “anterior cingulate circuit”. In their paper defining these Although oversimplifications can clearly be misleading, a two circuits Alexander et al4 note that this list is unlikely to be word summary of the role of the basal ganglia that may be exhaustive and that there may well be additional parallel cir- helpful in considering this region is that these structures are cuits whose identification is currently precluded by the lack of involved in “psychomotor behaviour”.13 More detailed consid- appropriate data. erations have proposed that the basal ganglia serve a compu- Each circuit receives multiple corticostritate inputs that are tational role,14 15 with each component being part of highly progressively integrated in their passage through the basal complex and widely distributed neural networks in which ganglia, ultimately to a restricted area of the thalamus and sequences “of activation and inhibition are coded in both time from there back to a single cortical area. It has been concluded and space with exquisite precision”. “This network endows that in each of these circuits an important function is the the brain with a high level of neural plasticity necessary to integration or funnelling of multiple corticostritate inputs modulate motor behaviour in a subtle manner and to back to a single cortical area. It is also concluded that the overcome motor deficits through ingenious strategies”.9 multiple cortical areas that input into each circuit are Functions in which the basal ganglia seem to be involved functionally related to each other and also usually include motor learning, sequencing, and movements, atten- 4 interconnected. This pattern of organisation also seems to tional allocation and filtering, working memory, and implicit apply to the other output nucleus from the basal ganglia, the 5 learning and memory. These operations may play a part in pars reticulata of the substantia nigra. both the acquisition of behaviours that are performed Examining connections between the basal ganglia and pre- 67 automatically and in enhancing the efficiency of higher order frontal cortex has led to the following conclusions. Firstly, processors such as those involved in working memory.16 several areas of the prefrontal cortex that are involved in There is also evidence that the basal ganglia may have an higher order cognitive function, particularly some aspects of important role in reward processes.17 Rewards elicit approach working memory, are targets of output from the basal ganglia. and consummatory behaviour. They increase the frequency and Secondly, the basal ganglia output channels related to cortical intensity of behaviour leading to such outcomes, serving as motor areas are topographically separate from those project- positive reinforcers. Dopaminergic pathways have been shown ing to areas of prefrontal
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