Elsevier

Neuropsychologia

Volume 38, Issue 5, 1 May 2000, Pages 613-627
Neuropsychologia

Neuropsychology of infarctions in the thalamus: a review

https://doi.org/10.1016/S0028-3932(99)00104-9Get rights and content

Abstract

From a review of the literature on the consequences of thalamic infarctions, it may be concluded that memory problems taking the form of an amnesic syndrome are dependent upon the integrity of the mammillo-thalamic tract (MTT). Memory problems incompatible with an amnesic syndrome however, appear to result from thalamic infarctions involving other areas of the thalamus but which leave MTT intact. In contrast, executive dysfunctions could not be shown so readily to depend upon a single structure of the thalamus. The results indicate that damage to the mediodorsal nucleus of the thalamus, the midline nuclei or the intralaminar nuclei, or a combined lesion of these structures may be responsible for deficits of executive functioning.

Introduction

It has long been recognized that lesions in the thalamic region, be they of either vascular, tumorous or traumatic origin, can cause cognitive disturbances [14], [59], [73]. Traditionally, the memory loss associated with such lesions received most attention and is usually described as ‘diencephalic amnesia’ [29], [82]. This term suggests that there is a consistent symptomatology across patients but in fact the pattern of memory deficits can be very different among patients with thalamic lesions. In addition, in recent years reports have stressed that, following damage to the thalamus, symptoms of a dysexecutive or ‘prefrontal’ type can occur alone or in combination with memory loss [13], [19], [50], [60], [79]. The current article attempts to give an overview of (a) the different memory deficits and (b) the executive deficits following thalamic lesions.

The pattern of memory loss occurring in patients with lesions of the thalamic region has traditionally been thought to resemble that seen after lesions in the medial temporal lobe (MTL) region [1]. The memory problems of patients with MTL lesions typically take the form of an amnesic syndrome due to defective encoding of new information, resulting in impaired anterograde memory with intact short-term memory and normal intelligence [84]. Recent data have indicated, however, that damage to certain areas within the MTL may result in retrieval rather than encoding difficulties [1]. Nevertheless, in this article MTL functioning is taken as a whole since the functional differentiation within the MTL does not translate to a differentiation in the thalamus [86] and therefore we regard retrieval and encoding deficits as part of a thalamic MTL-like amnesia.

It should be noted that memory disturbances other than the amnesic syndrome are also frequently encountered in thalamic-lesioned patients and other neurological patients. Such disturbances may for instance result from inattention. It is often quite difficult to distinguish between the amnesic syndrome and other memory problems with the use of neuropsychological tests.

Nevertheless, in this article, the difference between these miscellaneous forms of memory dysfunction and the amnesic syndrome (the latter to be used interchangeably with MTL-like amnesia henceforth) is thought to be of importance in the description of the role of thalamic function in memory processes and we have attempted to operationalise the differentiation between the two as described below in the section ‘selection of cases’.

As mentioned above, lesions in the thalamus not only give rise to memory problems but also lead to the disruption of processes which are ascribed to the prefrontal cortex (PFC). ‘Prefrontal’ symptoms include disturbances of executive abilities, attention, initiative, inhibition and temporal organization of behaviour [23], [24], seen in cases of patients with lesions of the PFC. In such cases, the precise pattern of deficits seems to depend on the area of the PFC that is lesioned. Dysfunctions of the medial part of the PFC result in apathy and lesions in the orbital PFC are responsible for behavioral disinhibition [20]. Structural lesions in the dorsolateral PFC affect executive functions, as evidenced by a lack of planning of behavior, an impairment of serial ordering, a deficit of attentional capacities, and severe distractibility [24].

There is evidence that the frontal cortex also actively participates in memory processes, namely the retrieval of information and the use of search strategies in the memory store [36], [48], [71]. Imaging studies have shown that the frontal cortex is activated during encoding [77], but it has not yet been established whether this activation is crucial for the formation of new memory traces. Therefore, memory problems may arise either as a direct consequence of prefrontal damage or secondarily as a result of prefrontal cognitive deficits, for example, inattention. The resulting ‘prefrontal memory problems’ can be distinguished from MTL-like amnesia by using neuropsychological tools, since recognition or aided retrieval is often spared, whereas active recall from the memory store is impaired [67]. However, it should be clear that executive dysfunctions and the amnesic syndrome can occur together in patients with extensive thalamic damage.

The understanding of cognitive effects of thalamic lesions has been hampered because of the small number of patients with such lesions. Most descriptions of diencephalic amnesia have been case studies, which makes it difficult to compare results because different neuropsychological tests were often used. Also, it has only recently become possible, with the advent of magnetic resonance imaging (MRI), to localize the lesion more precisely. The importance of spatial resolution in delineating the site of thalamic infarctions can be appreciated by considering the size of the various thalamic structures [35], [53]. Some of the separate nuclei have volumes of only a few cubic millimeters, and since each nucleus has its own specific pattern of inputs and outputs [74], the effect of a lesion will depend upon subtle differences in its location.

This lack of neuropsychological data and of accurate anatomical localization of the thalamic lesion, means that it is not yet clear which structures are involved in the amnesic symptoms encountered following such a lesion [8]. In addition, it is unknown which thalamic structures are responsible for the disruption of typical prefrontal processes. The aim of this article is therefore to provide a detailed review of reports of the effects of selective lesions of parts of the thalamus, in order to gain an insight into the contribution of the thalamic substructures to cognitive functioning. The review focuses on the elements common to all cases described in the neurological and neuropsychological literature over the past two decades.

Section snippets

Selection of cases

Thirty-five articles involving a total of 60 patients were selected from the international literature since 1980 on the basis of three criteria. First, lesions had to be restricted to the thalamus and had to result from lacunar infarctions because the effects of these lesions are more spatially restricted than those of haemorrhages, traumata or tumors. Second, the article had to contain a description of the procedure used to delineate the structures of the thalamus that were affected by the

Memory dysfunction after thalamic infarction

The evidence for disruption of memory and other cognitive functions is discussed on the basis of the studies listed in Table 1.

Influential reports on the nature of diencephalic amnesia [29], [82] have stressed that the fiber system of the mammillo-thalamic tract (MTT) rather than nuclear structures in the thalamus is responsible for anterograde memory. Several studies have since confirmed the notion that anteriorly, but not posteriorly, located infarctions can cause a profound amnesic syndrome.

Limitations of the data

As can be seen from Table 2, clinical memory research usually emphasizes performance in short-delay tests. Little attention has been paid to performance in long-delay tests and even less to tests of recognition memory. However, especially in patients with unilateral lesions, in whom the neuropsychological deficit is often either verbal or non-verbal, short-term retention, long-term retention and recognition should be tested in the same modality to allow a diagnosis of MTL-like anterograde

Memory dysfunction after thalamic infarction

On the basis of the articles reviewed, the occurrence of an amnesic syndrome is associated with lesioning of the MTT, regardless of whether the infarction is in the anterior or middle thalamus. Only in one patient [15] was an amnesic syndrome not accompanied by destruction of this fiber tract. Conversely, nearly all the patients who did not have memory problems compatible with an amnesic syndrome had an intact MTT (11 vs 2) (Table 3).

The conclusion seems wholly compatible with the ideas

Thalamic contribution to cognition in the light of neuroanatomical data

The medial thalamus is widely regarded to be the region of the thalamus involved in the formation of memories. The medial thalamus comprises several structures, including the IML, Midline nuclei, MD, the anterior nuclei and the MTT. No conclusive evidence has been presented concerning which of these medial thalamic structures is crucial for anterograde memory [8].

Amnesia due to thalamic damage has classically been regarded as a disconnection syndrome [83], taken as a disconnection of the

Conclusions

It is clear from the reviewed literature that the thalamus participates in many brain circuits involved in the processing of old information and new stimuli, which allows it to influence behavior, complex cognitive skills, and memory processes. Although we now have some insight into which structures of the thalamus, both nuclei and fiber tracts, are involved in these faculties, a full picture has not yet emerged. This is in part due to the variable quality of neuropsychological testing of

Acknowledgements

This study was supported by a grant from the Netherlands Organization for Scientific Research (NWO), grant number 970-10-012.

References (88)

  • H.J. Markowitsch

    Diencephalic amnesia: a reorientation towards tracts?

    Brain Research Reviews

    (1988)
  • H.J. Markowitsch

    Which brain regions are critically involved in the retrieval of old episodic memory?

    Brain Research Reviews

    (1995)
  • B. Milner et al.

    Behavioural effects of frontal-lobe lesions in man

    Trends in Neurosciences

    (1984)
  • A.J. Parkin et al.

    Impairment of memory following discrete thalamic infarction

    Neuropsychologia

    (1994)
  • A. Peru et al.

    Thalamic amnesia following venous infarction: evidence from a single case study

    Brain and Cognition

    (1997)
  • L.J. Speedie et al.

    Amnestic disturbance following infarction of the left dorsomedial nucleus of the thalamus

    Neuropsychologia

    (1982)
  • D.T. Stuss et al.

    The neuropsychology of paramedian thalamic infarction

    Brain and Cognition

    (1988)
  • E.K. Warrington et al.

    Amnesia: a disconnection syndrome?

    Neuropsychologia

    (1982)
  • G. Winocur et al.

    Amnesia in a patient with bilateral lesions to the thalamus

    Neuropsychologia

    (1984)
  • J.P. Aggleton et al.

    The relationships between temporal lobe and diencephalic structures implicated in anterograde amnesia

    Memory

    (1997)
  • J.P. Aggleton et al.

    The origin, course, and termination of the hippocampothalamic projections in the macaque

    Journal of Comparative Neurology

    (1986)
  • G.V. Allen et al.

    Mamillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex, and the midbrain tegmentum

    Journal of Comparative Neurology

    (1989)
  • C.R. Archer et al.

    Aphasia in thalamic stroke: CT stereotactic localization

    Journal of Computer Assisted Tomography

    (1981)
  • J.C. Baron et al.

    Effects of thalamic stroke on energy metabolism of the cerebral cortex. A positron tomography study in man

    Brain

    (1986)
  • J.C. Baron et al.

    Thalamocortical diaschisis: positron emission tomography in humans

    Journal of Neurology Neurosurgery and Psychiatry

    (1992)
  • F. Barontini et al.

    Isolated amnesia following a bilateral paramedian thalamic infarct. Possible etiologic role of a whiplash injury

    Acta Neurologica

    (1992)
  • M. Bentivoglio et al.

    The thalamus and memory formation

  • 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.

    The syndrome of unilateral tuberothalamic artery territory infarction

    Stroke

    (1986)
  • J. Bogousslavsky et al.

    Loss of psychic self-activation with bithalamic infarction. Neurobehavioural, CT, MRI and SPECT correlates

    Acta Neurologica Scandinavica

    (1991)
  • J. Bogousslavsky et al.

    Thalamic infarcts: clinical syndromes, etiology and prognosis

    Neurology

    (1988)
  • P. Calabrese et al.

    The cognitive mnestic performance profile of a patient with bilateral asymmetrical thalamic infarction

    International Journal of Neuroscience

    (1993)
  • S. Clarke et al.

    Pure amnesia after unilateral left polar thalamic infarct: topographic and sequential neuropsychological and metabolic (PET) correlations

    Journal of Neurology Neurosurgery and Psychiatry

    (1994)
  • I. Daum et al.

    Dissociation of declarative and nondeclarative memory after bilateral thalamic lesions: a case report

    International Journal of Neuroscience

    (1994)
  • I. Daum et al.

    Frontal-type memory impairment associated with thalamic damage

    International Journal of Neuroscience

    (1994)
  • J.D. Duffy et al.

    The regional prefrontal syndromes: a theoretical and clinical overview

    Journal of Neuropsychiatry and Clinical Neurosciences

    (1994)
  • C. Fensore et al.

    Language and memory disturbances from mesencephalothalamic infarcts. A clinical and computed tomographic study

    European Neurology

    (1988)
  • J.M. Fuster

    Frontal Lobe Syndromes

  • J.M. Fuster
  • M. Gentillini et al.

    Bilateral paramedian thalamic artery infarcts: report of eight cases

    Journal of Neurology Neurosurgery and Psychiatry

    (1987)
  • G. Goldenberg et al.

    Amnesic syndrome with a unilateral thalamic lesion: a case report

    Journal of Neurology

    (1983)
  • P.B. Gorelick et al.

    Transient global amnesia and thalamic infarction

    Neurology

    (1988)
  • N.R. Graff-Radford et al.

    Nonhemorrhagic infarction of the thalamus: behavioral, anatomic, and physiologic correlates

    Neurology

    (1984)
  • N.R. Graff-Radford et al.

    Diencephalic amnesia

    Brain

    (1990)
  • Cited by (292)

    • Specific structuro-metabolic pattern of thalamic subnuclei in fatal familial insomnia: A PET/MRI imaging study

      2022, NeuroImage: Clinical
      Citation Excerpt :

      Among all the thalamic nuclei, the medial dorsal nucleus is one of the higher order for its close anatomical relationship with the entire prefrontal cortex and as it also receives broad spectrum of afferent projections from the areas involved in regulation of sleep wake cycle (Van der Werf et al., 2002). Lesions within this nucleus may release the subcortical and brainstem regions from forebrain cortical control, which leads to autonomic, motor activation and “prefrontal-like” dysexecutive symptoms (Montagna, 2011; Van der Werf et al., 2000). The hyperactivity of the reticular regions of the brainstem could also result in insomnia, and loss of sleep spindles (Jan et al., 2009; Montagna, 2011).

    View all citing articles on Scopus
    View full text