Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions

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Abstract

The thalamus plays a crucial role in memory, executive functioning and attention. It remains, however, unclear whether thalamic structures have specific roles in each of these functions. We tested 22 cases of thalamic infarction, proven with MR imaging, using experimental and established neuropsychological tests. We performed a lesion-overlap study in standardised stereotactic space of patients sharing a certain deficit, corrected for the lesion distribution of patients without such deficits and determined the regions of interest using an atlas of the human thalamus. We checked for additional, non-thalamic, damage and for deficient comprehension and perception that would preclude interpretation of the results. Non-thalamic damage such as white matter lesions, hippocampal atrophy, sulcal widening and infarctions occur significantly more often in patients aged over 60. The patients with additional damage overlapped to a major degree with those who showed loss of orientation, or lack of comprehension of the test requirements. In the 10 patients judged ‘clean’, we observed a deficit of episodic long-term memory with relative sparing of intellectual capacities and short-term memory when the mammillo-thalamic tract was damaged. Lesions including the medial dorsal nucleus, midline nuclei and/or intralaminar nuclei accompany executive dysfunctioning. Reduced simple processing speed and attention are associated with age, but not with a particular structure in the thalamus. Complex attention deficits follow damage to the intralaminar nuclei.

We conclude that the analysis of structure–function relationships must take into account extra-structure damage which may explain cognitive deficits. Separate thalamic structures are involved in memory, executive functioning and attention.

Introduction

Studies of patients with thalamic damage show that the thalamus plays a role in several aspects of cognition. Of these, memory has always received the greatest attention due to striking cases of diencephalic amnesia, i.e. severe memory loss due to thalamic damage (Bogousslavsky et al., 1988, Bogousslavsky et al., 1988; Castaigne et al., 1981; Ghidoni, Pattacini, Galimberti, & Aguzzoli, 1989; Graff-Radford, Damasio, Eslinger, Yamada, & Damasio, 1985; Neau & Bogousslavsky, 1996; Partlow, Del Carpio-O’Donovan, Melanson, & Peters, 1992; Rousseaux, 1994, Rousseaux et al., 1986; Stuss, Guberman, Nelson, & Larochelle, 1988; Wallesch, Kornhuber, Kunz, & Brunner, 1983). This memory deficit depends on damage to the medial and anterior portions of the thalamus (Graff-Radford, Tranel, Van Hoesen, & Brandt, 1990; Von Cramon, Hebel, & Schuri, 1985); more precisely, the anterograde amnesia, reminiscent of that seen following hippocampal damage, in cases with thalamic damage appears to follow lesions of the anterior thalamic nuclei or their afferent white matter bundle, the mammillo-thalamic tract (Gentillini, De Renzi, & Crisi, 1987; Van Der Werf, Witter, Uijlings, & Jolles, 2000). Severe deficits in executive functioning and attention have also been noted in thalamic patients, but it remains unclear which structures are involved (Bogousslavsky et al., 1988, Bogousslavsky et al., 1988; Fukatsu, Fujii, Yamadori, Nagasawa, & Sakurai, 1997; McGilchrist, Goldstein, Jadresic, & Fenwick, 1993; Miller, Cummings, McIntyre, Ebers, & Grode, 1986; Pepin & Auray-Pepin, 1993; Sandson, Daffner, Carvalho, & Mesulam, 1991; Van Der Werf et al., 1999).

We here present a study of 22 cases of thalamic infarction, tested with a fixed battery of tests to allow comparison between cases. The selection of tests aimed to measure different aspects of memory, attention and executive functioning. We obtained MRI scans from each patient and plotted the lesion sites both in standard stereotactic space and in an atlas of the thalamus. This allowed us on the one hand to perform an analysis of the overlap of infarctions in groups of patients with similar symptoms and on the other hand, we were able to describe the location of the regions of interest in terms of nuclei and white matter tracts affected. We controlled for infarctions in subcortical areas and white matter tracts surrounding the thalamus, hippocampal atrophy and sulcal widening, factors that would confound structure–function relationships within the thalamus (De Groot et al., 2000; Houx, Vreeling, & Jolles, 1991; Scheltens et al., 1992, Visser et al., 1999). Similarly, we controlled for deficits of basal cognitive abilities, such as vigilance and understanding. In doing so, we aimed to provide more information on which thalamic structures are involved in executive functioning and attention, and to confirm previously established structure–function relationships for memory (Van Der Werf et al., 2000).

Section snippets

Methods

Neurologists from four academic centres in The Netherlands participated to recruit patients with thalamic stroke from neurology clinics, rehabilitation clinics, academic hospitals and community hospitals. In the course of 4 years, 22 patients were included.

In all patients, the diagnosis of thalamic infarction was made with the aid of structural brain images; in most cases, high-resolution MR images were obtained with a 1.5 T machine using both T1- and T2-weighted images. In case 11, no MR

Thalamic lesions

Of the 22 patients studied, 15 had unilateral lesions and 7 had lesions falling in the thalamus of both hemispheres. The latter type of infarction was more or less symmetrical in three cases, but four cases had lesions that were larger on one side or in different locations on each side. Table 3 lists the nuclei affected and Fig. 2 illustrates the location, size and shape of the lesions.

Recurring patterns occurred in the distribution of lesions: eight patients showed an elongated lesion in the

Discussion

We aimed to find relationships between thalamic structures and memory, executive functions and attention. We performed a lesion-overlap and subtraction study in stereotactic space to investigate associations between thalamic structures and cognitive functions across our group of subjects, followed by a case-wise analysis of the pattern of deficits in each subject. A clear relationship between a specific kind of memory disorder, i.e. the amnesic syndrome, and structural damage to the MTT was

Acknowledgments

This study was supported by a grant from The Netherlands Organisation for Scientific Research (NWO), Grant Number 970-10-012. The help of Drs. W.J.H.J. Smeets and H.J. Groenewegen for lesion localisation and of Drs. Barkhof, Boiten, Gonera, Haaxma and Weerts for referral of patients is gratefully acknowledged.

References (66)

  • S.F. Taylor et al.

    Isolation of specific interference processing in the Stroop task: PET activation studies

    Neuroimage

    (1997)
  • Y.D. Van Der Werf et al.

    Thalamic volume predicts performance on tests of cognitive speed and decreases in healthy aging. A magnetic resonance imaging-based volumetric analysis

    Cognitive Brain Research

    (2001)
  • Y.D. Van Der Werf et al.

    Neuropsychology of infarctions in the thalamus a review

    Neuropsychologia

    (2000)
  • J.P. Aggleton et al.

    Episodic memory, amnesia and the hippocampal-anterior thalamic axis

    Behavioral and Brain Sciences

    (1999)
  • E.A. Berg

    A simple objective treatment for measuring flexibility in thinking

    Journal of General Psychology

    (1948)
  • J. Bogousslavsky et al.

    Manic delirium and frontal-like syndrome with paramedian infarction of the right thalamus

    Journal of Neurology, Neurosurgery and Psychiatry

    (1988)
  • J. Bogousslavsky et al.

    Thalamic infarcts: Clinical syndromes, etiology and prognosis

    Neurology

    (1988)
  • N. Brand et al.

    Learning and retrieval rate of words presented auditorily and visually

    Journal of General Psychology

    (1985)
  • N. Brand et al.

    Information processing in depression and anxiety

    Psychological Medicine

    (1987)
  • Brickenkamp, R. (1981). Test d2 Aufmerksamkeits-Belastungs-Test. Göttingen (Germany):...
  • P. Castaigne et al.

    Paramedian and midbrain infarcts: Clinical and neuropathological study

    Annals of Neurology

    (1981)
  • J.C. De Groot et al.

    Cerebral white matter lesions and cognitive function: The Rotterdam Scan Study

    Annals of Neurology

    (2000)
  • N.M.J. Edelstyn et al.

    Contribution of the left dorsomedial thalamus to recognition memory: A neuropsychological case study

    Neurocase

    (2002)
  • R. Fukatsu et al.

    Persisting childish behavior after bilateral thalamic infarcts

    European Neurology

    (1997)
  • M. Gentillini et al.

    Bilateral paramedian thalamic artery infarcts: Report of eight cases

    Journal of Neurology, Neurosurgery and Psychiatry

    (1987)
  • E. Ghidoni et al.

    Lacunar thalamic infarcts and amnesia

    European Neurology

    (1989)
  • N.R. Graff-Radford et al.

    Nonhaemorrhagic thalamic infarction. Clinical, neuropsychological and electrophysiological findings in four anatomical groups defined by computerized tomography

    Brain

    (1985)
  • N.R. Graff-Radford et al.

    Diencephalic amnesia

    Brain

    (1990)
  • Hofman, P. A. M. (2000). Brain imaging in mild traumatic brain injury and neuropsychiatric disorders: A quantitative...
  • P.J. Houx et al.

    Age-related decline of psychomotor speed: Effects of age, brain health, sex, and education

    Perceptual and Motor Skills

    (1993)
  • Jolles, J. (1986). Cognitive, emotional and behavioral dysfunctions in aging and dementia. In: D. F. Swaab, E. Fliers,...
  • Jolles, J., Houx, P. J., Van Boxtel, M. P. J., & Ponds, R. W. H. M. (Eds.). (1995). The Maastricht aging study....
  • H.-O. Karnath et al.

    The subcortical anatomy of human spatial neglect: Putamen

    Brain

    (2002)
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