Subcortical Dementia{{ the Evolution of the Concept

BRITISH JOURNAL OF PSYCHIATRY #2002),#2002),180,148^151 180, 148^151

Subcortical dementia{{ The evolution of the concept

In 1872, at a time when dementia was a MARK A. TURNER, NICHOLAS F. MORAN and MICHAEL D. KOPELMAN unitary concept, Huntington published `On Chorea', describing the cognitive impairments in the disease that bears his name. In 1874 Meynert, whose interests were both clinical and neuroanatomical, publishedpublished Psychiatry: A Clinical Treatise on Diseases of the Forebrain Based upon its Structure, Function and its Nutrition.. In this book he sought to relate brain struc- Background Drawing a distinction The concept of subcortical dementia devel- ture to function, and postulated that certain between cortical and subcortical oped out of clinical observations of de- psychiatric symptoms resulted from an mentia in the context of disease processes imbalance of blood flow between the sub- dementias seems both useful andjustified. preferentially affecting the subcortical cortical and cortical structures. Meynert Recent research has, however, castdoubt structures. The syndrome was claimed to may have been mistaken in making his on the clinical, neuropsychological, be distinct in its clinical manifestations emphasis on blood flow, but if he had neuroimaging and neuroanatomical basis and its anatomicopathological correlates. talked in neural terms instead, he would of the distinction. The dichotomy between cortical and sub- surely have pre-empted current thinking cortical dementias has now come under about the aetiology of subcortical demen- Aims Toarrive at a reasoned conclusion attack from both the neuropsychological tia. In 1894 Binswanger introduced a aboutaboutthe the relationship between the two and neuroanatomical perspectives. vascular perspective and characterised encephalitis subcorticalis chronica pro- types of dementia and the validity of gressivagressiva, subsequently renamed subcortical distinguishing between them. arteriosclerotic encephalopathy by Olszewski BACKGROUND in 1962.in1962. MethodMethod The historical and recent In 1912 Wilson related subcortical clinical and scientific literature on Dementia is a degenerative disorder invol- disease to a clinical picture distinct from subcortical dementia was reviewed. ving the compromise of multiple domains that seen in cortical dementia when he of cognition. This definition excludes acute described cognitive impairments in the ResultsResults The traditional claimthat confusion of any cause and also chronic absence of apraxia and agnosia in cases of subcortical dementia has distinctclinical focal brain syndromes, in particular the `progressive lenticular degeneration: a manifestations, neuroimaging findings and amnesic syndrome. The further classifica- familial nervous disease associated with tion of dementia, whether based on clinical cirrhosis of the liver', commonly known a neuropathological profile is not presentation or on aetiology, is, however, nowadays as Wilson's disease. Sub- altogether borne out by the literature. fraught with difficulties. Despite this, the sequently a number of other predominantly Some studies show thatfrontal executive emerging view since the mid-1970s has subcortical disease processes have been dysfunction and the profile of memory been that dementia can be separated into characterised and found to be associated cortical and subcortical types, a distinction with a pattern of cognitive impairment that deficits are not significantly different from that has found support from both the clini- supports the idea of distinction between those seenseenin in Alzheimer's disease. cal !Pilloncal!Pillon et aletal, 1993, for example) and cortical and subcortical dementias. Parkin- Neuropathological findings also overlap. aetiological perspectives !see Darvesh & son's disease was not formally incorporated Freedman, 1996, for a review). The differ- into the notion of subcortical dementia Conclusions The category of entiating features of subcortical dementia until 1978, following work by Albert, subcortical dementia may be clinically were said to be a profound slowing of cog- although debate about its aetiology and its usefulusefulin in highlighting the likelihood that an nition, memory disturbances, frontal execu- relationship with cognitive impairment individual with dementia is more likely to tive dysfunction, and changes in personality started as far back as 1932 when Von and affect in the absence of aphasias, Stockert introduced the term subcorticale suffer from bradyphrenia and motor apraxias and agnosias !Cummings, 1986). demenzdemenz to characterise the cognitive difficulties. As neuroscience advances a Other authors have highlighted the dif- impairment evident in a case of encephalitis preoccupation with the distinction may ficulties with the distinction by arguing that lethargica. Concerning more obscure hinder the assessment and treatment of the neuropsychological profiles of cortical causes, in 1938 Smyth and Stern had and subcortical cases are not sufficiently described cognitive impairment in the pre- individual cases. dissimilar !Brown & Marsden, 1988) or sence of thalamic disease. More recently, Declaration of interest None. that cortical abnormalities often occur in in 1974 Segarra and co-workers supported so-called subcortical disease !Hughes et aletal,, the contention that subcortical dementia 1993). With improvements in investigative can occur in the presence of isolated thala- techniques, notably neuroimaging, the mic disease, and in 1984 Katz also specu- ySee editorial, pp. 97^98, thisissue. debate about this matter is likely to continue. lated that the dementia associated with

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multi-system atrophy may be of thalamic dysfunction and impairment in memory there is a learning impairment which can origin.origin. characteristic of subcortical dementia may be partially corrected by providing richer Although McHugh apparently used the be present.bepresent. !more salient) cues to encourage learning term `subcortical dementia' to characterise The psychiatric manifestations of sub- and promote recognition !Pillon et aletal,, the deficits seen in Huntington's disease in cortical disease come primarily in the form 1993). In contrast, it was claimed that an unpublished communication in 1973, it of personality changes and affective dis- cortical dementias !such as Alzheimer's was Albert and colleagues in 1974 who order. Apathy and irritability are particu- dementia) are characterised by accelerated formally articulated the concept: in a dis- larly common !Aarsland et aletal, 1999), and forgetting !e.g. Cummings, 1986). cussion of the cognitive impairments associ- depression is said to be significantly more However, this distinction does not hold ated with progressive supranuclear palsy, common in subcortical disorders such as good on detailed neuropsychological AlbertAlbert et aletal !1974) specified the clinical Parkinson's disease than it is in Alzheimer's analysis of the patterns of learning and features of the syndrome for the first time. disease. Aarsland et aletal !1999) found that forgetting in, for example, Huntington's Subsequently, a similar clinical picture 38% of a series of patients with Parkinson's disease and Alzheimer's dementia was described in association with basal disease had depression, and Cummings !Kopelman, 1985), and Kuzis et aletal !1999)!1999) ganglionic calcification in hyperpara- !1995) gave a figure of 30% for Hunting- could not demonstrate a different profile thyroidism by Bachman & Albert !1984) ton's disease that is broadly in keeping with of memory deficits between patients with and in human immunodeficiency virus the figure of 41% reported by Dewhurst Alzheimer's dementia and those with dementia by Navia et aletal !1986). There are et aletal !1969) for their series of Huntington's dementia consequent upon Parkinson's a number of other neurological disorders, cases. Psychotic illness and mania are also disease. In remote memory, there are including normal pressure hydrocephalus, overrepresented, particularly in Hunting- variable patterns of impairment. In Alz- the `pugilistic encephalopathy' of repeated ton's disease: psychotic illness was present heimer's dementia a gentle `temporal head injury, multiple sclerosis and the in over 50% and mania in 21% of the gradient' !an extensive remote memory loss spinocerebellar degenerations, that can be Dewhurst series, and in the Parkinson's with some degree or relative sparing of postulated as subcortical dementias but disease series 27% had hallucinations early memories) is found in many studies are not mentioned again here. From the !Aarsland!Aarsland et aletal, 1999).,1999). !Kopelman, 1989), although there have psychiatric perspective, there are similari- In terms of cognition, some evidence been claims that this is specific for auto- ties between the clinical features of sub- suggests that cortical dementia evolves biographical memories as opposed to cortical dementia and those of depressive differently from subcortical dementia. Stern memories of famous events !Dorrego et aletal,, pseudodementia !Caine, 1981) and type II et aletal !1998) evaluated cognitive changes 1999), whereas in Huntington's disease schizophrenia !Pantelis et aletal, 1992).,1992). over 1±3 years prior to the time dementia there is a `flat', uniform loss of remote was diagnosed in 40matched pairs of memories across all earlier periods. In patients with Alzheimer's disease and Parkinson's disease, the severity of remote CLINICAL AND Parkinson's disease. The study showed that memory impairment is related to the NEUROPSYCHOLOGICAL the decline in naming on the Boston clinical severity of dementia; however, MANIFESTATIONS Naming Test !Kaplan et aletal, 1983) and in these patients additionally seem to have performance on the Selective Reminding difficulty in dating past events, even when In Alzheimer's disease senile plaques and Test !Buschke & Fuld, 1974) was more they do not suffer from formal dementia. neurofibrillary tangles populate the cortex rapid in Parkinson's disease than in There have been many studies of and there is generalised cortical atrophy, Alzheimer's disease, which Stern and procedural !perceptuomotor) learning in especially of the frontal and temporal lobes, colleagues felt was in keeping with different Parkinson's disease and Huntington's with neuronal degeneration affecting par- underlying pathological processes. dementia. Saint-Cyr et aletal !1988) found that ticularly the outer three layers. The typical In terms of the actual pattern of deficits, in both conditions patients were impaired clinical findings include dyscalculia, dys- slow thinking !bradyphrenia) has been at the Tower of Hanoi task, whereas phasias, dyspraxias and agnosias, and are demonstrated in both Parkinson's disease amnesic patients performed normally !on said to be indicative of cortical dysfunction. and Huntington's disease and is indepen- the basis of the latter's intact procedural However, features reflecting subcortical dent of attendant motor slowness. Frontal/ memory); on verbal memory tasks, in pathology, such as mild extrapyramidal executive function, as evidenced by difficul- contrast, the amnesic patients were severely signs, are common. ties with verbal fluency, set shifting, cate- impaired, whereas those with Parkinson's In the subcortical dementias, on the gorisation and planning, is also disturbed disease performed normally and those with other hand, the lesions occur pre- in all the major subcortical diseases !Elias Huntington's disease showed a variable dominantly in the basal ganglia, the brain- & Treland, 1999). It is also impaired in pattern. More recently, Reber & Squire stem nuclei and the cerebellum !see early Alzheimer's dementia !Kopelman, !1999) have demonstrated that skill Darvesh & Freedman, 1996, for a compre- 1991). There is evidence to suggest that learning is not a single entity: patients with hensive review of the neuroanatomy and patients with early Alzheimer's disease are Parkinson's are impaired at `habit' learning, neuropathology), and the clinical picture disproportionately impaired in category implicating the neostriatum, but show is correspondingly different. In addition to fluency as compared with letter fluency, a intact learning of artificial grammars and the clinical features of the underlying fact that comfortably fits with more severe dot pattern prototypes, which were disease process !whether it be Parkinson's, semantic memory problems in the former. postulated to reflect brain regions outside Huntington's or other disease) psychiatric In subcortical dementia !e.g. in Parkin- both the neostriatum and the medial disturbance, bradyphrenia, frontal executive son's disease and Huntington's dementia), temporal lobes.

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SUBCORTICAL thereby raising the interesting question of nucleus basalis of Meynert, a finding CONTRIBUTION TO whether or not depression and the sub- corroborated by many others. PSYCHIATRIC DISORDER? cortical dementias share a common or Neuroimaging findings in some studies closely related aetiology. There is support add further weight to the idea that the For the purposes of investigating cognitive for this hypothesis from both the neuro- dichotomy is not strict. Starkstein et aletal impairments in depression, Caine !1981) pathological and the functional imaging !1997), for example, compared patients defined `pseudodementia' as follows: perspectives. In patients with Parkinson's with Alzheimer's and Parkinson's disease !a)!a)itit is an intellectual impairment in a disease who had both depression and with dementia with patients with Parkin- patient with a primary psychiatric dementia, Ring et aletal !1994), for example, son's disease without dementia, using disorder;disorder; found hypometabolism in the medial pre- single-photon emission computed tomo- frontal cortex using positron emission graphy !SPECT). They found that the two !b)!b)thethe features of the neuropsychological tomography !PET), suggesting that groups with dementia did not differ signifi- disorder resemble, at least in part, the frontal/subcortical changes may contribute cantly from each other, but showed signifi- presentation of a neuropathologically induced cognitive deficit; to !or reflect) depressed mood in this cantly more severe hypoperfusion in the disorder.disorder. superior frontal, superior temporal and !c)!c)thethe intellectual disorder is reversible; In type II schizophrenia, Pantelis et aletal parietal areas than did those without !d)!d)thethe patient has no apparent primary !1992) addressed the question of whether dementia. As a consequence, any classifica- neuropathological process leading to the features that are similar to those seen tion of the dementias must be sensitive to the genesis of the disturbance. in subcortical dementia !such as apathy the fact that they seem to lie along a con- The disorder in question is usually and lack of motivation) should be taken tinuum involving a greater or lesser degree hysteria or depression but, because of the as evidence of a subcortical aetiology. In of cortical and subcortical pathology. additional complexities of understanding support of this, there is some neuropsycho- Even if one accepts the notion of a the mechanism of the former and how it logical and neuropathological evidence. In continuum, this still leaves a number of relates to the purposeful behaviour of terms of neuropsychology, Nelson et aletal unresolved issues. It is difficult to sustain malingering, attention is here confined to !1990), for example, showed a significant the idea that cortical dementia alone is depressive pseudodementia. negative correlation between cognitive characterised by some combination of Depression is common in subcortical speed and negative symptoms in patients aphasia, apraxia and agnosia, since apraxia disorders and it is perhaps not surprising with schizophrenia. The neuropathological is known to occur in disorders affecting the therefore that the pattern of cognitive evidence is less convincing, in spite of the basal ganglia. In addition, a number of impairment that one sees in the context of fact that a number of studies have revealed published care reports indicate that depression can be `subcortical'. As Lishman subcortical structural abnormalities in thalamic lesions sometimes produce demen- !1987: p. 410) eloquently puts it: schizophrenia. Recent work suggests that tia indistinguishable from Alzheimer's The patient becomes slow to grasp essentials, the loss of tissue is more general and that disease, and that frontal dysfunction ± said thinking is laboured, and behaviour becomes it may preferentially affect the cortex. The to be one of the characteristic features of generally slipshod and inefficient. Events fail to tentative conclusion is therefore that, while subcortical dementia ± is common in early register either through lack of ability to attend subcortical structures are likely to be Alzheimer's disease !Kopelman, 1991). and concentrate or on account of the patient's affected in schizophrenia and may be In conclusion, there is no specific inner preoccupations. In consequence he may responsible for some of the clinical features neuropsychological pattern in subcortical show faulty orientation, impairment of recent of the disorder, other regions of the brain dementia. However, the subcortical dis- memory, and a markedly defective knowledge of current events. The impression of dementia is are also affected. orders may still be more similar to one sometimes strengthened by the patient's another than they are to Alzheimer's decrepit appearance due to self-neglect or loss dementia. In so far as this is the case, they of weight. THE LEGITIMACY are characterised by cognitive slowness, To clarify the nature of the transient OF THE DISTINCTION concomitant motor abnormalities, and a cognitive impairments associated with relatively low frequency of aphasias and psychiatric disorder, Caine performed It is well-recognised that cortical abnormal- apraxias. When the latter occur, they reflect neuropsychological testing on a series of ities are frequently found in `subcortical' damage to subcortical±cortical projections. patients with pseudodementia and depres- diseases and vice versa. Hughes et aletal However, modern neuropsychology focuses sion. The results indicated a sparing of !1993) looked at 100 cases of histologically its attention on specific patterns of cog- `cortically mediated intellectual functions' confirmed Parkinson's disease and found nitive impairment in relation to underlying !Caine, 1981: p. 1363), including language that in 17 there was coexistent neuropatho- neurochemistry or neuropathology: to this functions and motor praxis, but difficulties logical evidence of Alzheimer-type change. extent, concepts such as `subcortical with inattention, slow mental processing In fact, dementia had occurred in 44% of dementia' are likely to blur, rather than to and a verbal elaboration `demonstrating a these patients and of these 29% had illuminate, our understanding. subcortical pattern of intellectual deficit' confirmed Alzheimer pathological change. !Caine, 1981: p. 1364). 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