Relevance of the cerebellar hemispheres for executive functions

doi:10.1016/S0887-8994(99)00128-9

Pediatric Neurology

Volume 22, Issue 2, February 2000, Pages 106-112

https://doi.org/10.1016/S0887-8994(99)00128-9 Get rights and content

Abstract

The aim of the present study was to elucidate the role of the cerebellar hemispheres in executive functions. The findings are relevant because of the large number of children who survive cerebellar tumors. Neuropsychologic assessments of four patients (8-21 years of age) who had undergone neurosurgery for removal of tumors in the cerebellar hemispheres were conducted and compared with the assessments of six children who had been diagnosed with temporal lobe tumors or cysts. The executive functions were assessed using the Wisconsin Card Sorting Test. IQs were average in both groups. As expected, patients with cerebellar hemispheric lesions had impaired executive functions. In particular, they appeared to have difficulty generating and testing hypotheses regarding the matching rules on the Wisconsin Card Sorting Test. Patients with temporal lesions had a different pattern of deficits on this test. The findings are consistent with the theories that propose that the cerebellar hemispheres are involved in cognitive processes. The findings also demonstrate that subtle deficits in executive functions can be masked by a normal IQ in survivors of cerebellar tumors and highlight the need to design interventions targeted toward problem-solving skills.

Introduction

Brain tumors are the second most frequent form of childhood cancer after leukemia. Because of improvements in medical imaging and treatment techniques, survivors of pediatric brain tumors are leading increasingly longer lives [1], [2]. Hence research is focused on improving long-term quality of life.

Astrocytomas are the most common type of pediatric tumor. A large proportion of astrocytomas develop in the cerebellum. Motor dysfunction is often the most obvious result of cerebellar damage. However, because the cerebellum has extensive connections with premotor, prefrontal, and paralimbic cortices, the thalamus, and the basal ganglia [3], [4], [5], [6], it is not surprising that higher-order cognitive deficits have been observed in children who had cerebellar tumors [7], [8], [9].

It has been hypothesized that the lateral cerebellum may play a role in cognitive functions and that the vermis may be involved in motor functions [4]. Consistent with this hypothesis, Allen et al. [10] determined that an attention task without motor requirements activated the left cerebellum and a motor task without attention requirements activated portions of the vermis and the right cerebellum. Neuropsychologic evidence was provided by studies of patients with cerebellar lesions who had impairments of executive functions traditionally associated with the frontal lobes [4], [11], [12]. Although no consensus has been reached on what constitutes an executive function, a list of these functions for many researchers would include planning, problem solving, decision making, encoding contextual information about stimuli, working memory, strategic and goal-directed behavior, abstract thought, cognitive flexibility, inhibition, judgment, adaptation to novel circumstances, and self-regulation.

Neuropsychologic studies of patients with cerebellar damage revealed deficits in tasks tapping executive functions, such as solving puzzles that require planning the most efficient way of rearranging the configuration of a set of objects according to certain rules [13], [14]. In normal humans, this task activates the dorsolateral, prefrontal, and frontopolar cortices and the dentate nucleus of the cerebellum [15], [16]. In another task that makes demands on problem solving but not on motor planning, normal adults were asked to generate hypotheses regarding the configuration of squares on a checkerboard [17]. Compared with guessing, hypothesis testing was associated with increased neural activity in the cerebellum, anterior cingulate, and prefrontal and posterior parietal cortices. Cerebellar activation was also observed during performance of the Wisconsin Card Sorting Test (WCST), which requires systematic problem solving but makes few demands on motor imagery or motor execution. In two studies of normal adults using positron emission tomography the cerebellum was activated during this task as part of a network that included the dorsolateral prefrontal, orbitofrontal, and parietal association cortices [18], [19].

However, the role of the cerebellum in executive functions is still in dispute. Normal to superior IQs in patients with cerebellar lesions have led some investigators [20] to conclude that “the cerebellum [is] not critically involved in general intellectual … abilities.” In addition, some studies report no impairment on executive function tests in adult patients with cerebellar lesions [13], [21], [22].

To examine the impact of lesions created by cerebellar tumors and their surgical removal on executive functions, four children who had tumors in the cerebellar hemispheres were examined. To determine the specificity of the results the findings were compared with six children who had temporal tumors or cysts. Executive functions were assessed using the WCST (described as follows).

Leiner et al. [4] observed that the lack of intellectual impairment in cerebellar patients may be because the deficits arising from cerebellar dysfunction “require subtle and detailed testing to detect.” A modest correlation between WCST performance and IQ has been observed [23]. Therefore, to exclude the effects of generalized intellectual dysfunction on WCST performance, WCST performances of the children were considered in the context of their individual IQs.

It was expected that participants with lateral cerebellar damage would demonstrate impairment on the WCST relative to their own IQs. Increases in activation in the inferolateral temporal cortex have been observed during performance of the WCST [18]. Therefore it was thought that the temporal patients might also demonstrate impairment on the WCST. However, in keeping with the idea of a distributed neural network for executive functions [24], it was thought that the temporal patients would differ in the pattern of their performances from the lateral cerebellar patients. The results highlighted the relevance of the cerebellar hemispheres for cognitive functions.

Section snippets

Participants

Children who had undergone complete removal of hemispheric cerebellar astrocytomas were recruited from the Pediatric Brain Tumor Clinic at the University of California, Los Angeles between 1996 and 1998. Children younger than 6 years of age, children with gross sensory-motor impairments, and patients whose cerebellar vermis was split during surgery were excluded. The demographic and medical characteristics of the participants are listed in Table 1. The group consisted of eight white and two

Results

Table 2 lists the scores on the Wechsler tests. Full-scale IQs ranged from average to high average (mean = 56th percentile, S.D. = 25), consistent with IQs observed in studies of nonirradiated children who had tumors in various regions of the brain [30], [31], [32], [33], [34]. There was also little difference between the full-scale IQs of the cerebellar and temporal groups (t = 1.46, P = 0.18).

The scores on the WCST are listed in Table 3. Following Lezak’s [35] suggestion regarding differences

Discussion

Compared with their own level of intelligence, three fourths of patients in the cerebellar group performed poorly on a test of executive function, with the fourth patient demonstrating a difference in the same direction. In the temporal group, only one patient had a trend toward more errors on the WCST than expected.

Although the sample size in this study was small, the impairment of children with lateral cerebellar damage on the WCST provided converging evidence for the hypothesis that the

Acknowledgements

We thank the participants and their families for taking part in the research project. We are grateful to Joshua Emerson, BA for preparing the drawings. This research was supported in part by a grant to Robert F. Asarnow, PhD from the Della Martin Foundation and by a grant to Jorge A. Lazareff, MD from the Friends of Pediatric Neurosurgery.

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Original ArticlesRelevance of the cerebellar hemispheres for executive functions

Abstract

Introduction

Section snippets

Participants

Results

Discussion

Acknowledgements

Surg Neurol

Prog Brain Res

Behav Brain Res

Prog Brain Res

Int Rev Neurobiol

Int Rev Neurobiol

Neuroimage

Neuropsychologia

Int Rev Neurobiol

Neuron

Neuropsychologia

Correlation of medical and neurosurgical events with neuropsychological status in children at diagnosis of astrocytomaUtilization of a neurological severity score

J Child Neurol

Assessment of quality of survival in children with medulloblastoma and cerebellar astrocytoma

Cancer

Preoperative and postoperative analysis of visual and auditory memory in children with cerebellar tumors

Childs Nerv Syst

Neuropsychological performance of children surviving cerebellar tumorsSix case studies

Int J Clin Neuropsychol

Attention activation of the cerebellum independent of motor involvement

Science

Movement and thoughtIdentical control mechanisms by the cerebellum

Trends Neurosci

Impaired non-motor learning and error detection associated with cerebellar damage

Brain

Cognitive planning deficit in patients with cerebellar atrophy

Neurology

Dissociating executive functions of the prefrontal cortex

Philos Trans R Soc Lond B Biol Sci

Activation of a cerebellar output nucleus during cognitive processing

Science

Original Articles
Relevance of the cerebellar hemispheres for executive functions