Does the cerebellum contribute to specific aspects of attention?

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Abstract

We present data on attentional and neuropsychological functions of 16 patients with focal cerebellar lesions (13 tumours, 3 haematomas) compared to normative test data, and to 11 control subjects matched for age, gender, and years of education. Patients showed distinct deficits in qualitative aspects of a divided attention task, and in a working memory task. Performance in selective attention was unimpaired. The results support the concept that the cerebellum plays a role not only in motor, but also in higher cognitive functions. They are discussed on the basis of the idea that prediction and preparation are fundamental functions of the cerebellum. Therefore, the results confirm the idea that cerebellar lesions lead to reduced performance in specific attention tasks.

Introduction

Although cerebellar abnormalities were found in different psychopathological diseases, such as autism, attention deficit hyperactivity disorder (ADHD), or schizophrenia, the image that the cerebellum possesses only motor functions has persisted. However, Carpenter (1991) describes a high rate of cerebellar afferents compared to the efferents (40:1). Considering this, it seems likely that this structure plays a highly integrative role in the brain. In the 1990s, there have been an increasing number of studies supporting the view that the cerebellum is involved in many different neuropsychological functions, including attention, independent of motor functions (Appollonio, Grafman, Schwartz, Massaquoi, & Hallett, 1993; Fiez, Petersen, Cheney, & Raichle, 1992; Grafman et al., 1992; Leggio, Silveri, Petrosini, & Molinari, 2000; Riva & Giorgi, 2000; Schmahmann & Sherman, 1998).

The term “attention” summarises different specific functions. Van Zomeren and Brouwer (1994) arranged the different functions along the two dimensions “intensity” and “selectivity”. The dimension “intensity” is subdivided into “alertness” and “sustained attention”. “Selectivity” is divided into “focused-attention” and “divided attention”. The relevant cortical structures for these functions are located within the right parietal and the prefrontal cortex, as well as in parts of the brainstem.

Another very complex term in this context is “working memory”, which is difficult to separate from attention. It can be seen in the context of the “supervisory attentional system” postulated by Shallice (1988) as being called upon in non-routine situations. The “supervisory attentional system” is a top-down process, consciously co-ordinating and reorganising new information. Anatomically the working memory is based on neural circuits connecting dorsolateral, ventrolateral and orbitofrontal structures (for more details, see Fletcher & Henson, 2001). If working memory is seen as a central executive organising new information, then a close connection to selective and divided attention seems obvious. Working memory, as well as selective and divided attention, are functions associated with frontal activity (Sturm & Zimmermann, 2000).

In 1998, Schmahmann and Sherman postulated the existence of a “cerebellar cognitive affective syndrome” (Schmahmann & Sherman, 1998). This syndrome implies an impairment of executive functions, disturbances in spatial cognition, language deficits, and personality changes. The deficits have been attributed to the disruption of the neural circuits linking prefrontal, temporal, posterior parietal and limbic cortices with the cerebellum. Since prefrontal and posterior parietal neural circuits are supposed to be crucial for attention, the close anatomical connections to the cerebellum indicate a cerebellar relevance for these functions as well.

Cerebellum and neocortex are strongly interconnected. Studies in non-human primates pointed out that the association areas of the posterior parietal cortex and prefrontal areas, both critical for focused attention, are connected via ventral pontine nuclei to the cerebellum. The limited information about ponto-cerebellar projections indicates that these pathways lead to the cerebellar hemispheres (Schmahmann & Pandya, 1997). Cerebellar output channels lead via the thalamus to multiple cortical areas. Middleton & Strick showed that these regions include premotor and prefrontal areas which are concerned not only with different aspects of motor, but also of cognitive behaviour. Several pathways originating from different regions of the nucleus dentatus were shown in neuroanatomical studies (Middleton & Strick, 1997).

There has also been evidence of neurofunctional activation of the cerebellum during attention tasks. Independent of motor aspects, cerebellar activity was shown by fMRI during a “focused-attention” task in the left superior posterior cerebellum (Allen, Buxton, Wong, & Courchesne, 1997). On the other hand, a motor task (right hand movement) in the same study activated the right anterior cerebellum. In “shifting-attention” tasks, using the “focused-attention” task as a control, activity was most prominent in the right lateral cerebellar hemisphere. In some subjects the ventral dentate nucleus was also activated (Le, Pardo, & Hu, 1998). Both studies proved a cerebellar contribution to attention totally independent of motor processes.

Further indications to a link between the cerebellum and attention come from studies describing morphological abnormalities in patients with attention deficit hyperactivity disorder (ADHD). ADHD is known as a disturbance of executive functions. It manifests itself in symptoms like inattention to stimuli that should lead to action, and defective response inhibition to those that should not. Anatomical correlates have been shown in the prefrontal cortex, in the basal ganglia, and in the cerebellum. Studies concerning anatomical features of the cerebellum, as measured by quantitative MRI, have shown smaller posterior inferior vermis lobules VIII–X in children with ADHD (Berquin et al., 1998, Castellanos et al., 2001). It seems likely that the posterior inferior vermal areas are part of a frontal-subcortical network relevant for the executive aspects of attention. On the other hand orienting and spatial shifting of attention could be based on a network including posterior superior vermal areas and the parietal cortex (Mostofski, Reiss, Lockhart, & Denckla, 1998).

Attention deficits are described in studies with autistic patients and cerebellar patients by Courchesne and colleagues (Akshoomoff, Courchesne, & Townsend, 1997; Ciesilski, Courchesne, & Elmasian, 1990; Courchesne & Allen, 1997; Harris, Courchesne, Townsend, Carper, & Lord, 1999; Townsend et al., 1999). In 95% of all autism autopsy cases cerebellar anatomic abnormality was present (Townsend et al., 2001). Most usually a hypoplasia of the vermal lobules VI and VII has been reported. Using quantitative MRI, Carper and Courchesne (2000) pointed out an inverse correlation between the size of the vermal lobules VI and VII and the frontal cortex in autistic patients. No such correlation was found in normal controls. They have proposed that anatomical abnormalities in one area of the cortex, i.e. the cerebellum, lead to the maldevelopment of another area, i.e. the frontal cortex. This dependence is in accord with reported crossed hemispheric diaschisis, a reduced blood flow predominant in the contralateral frontal region after unilateral cerebellar lesions (Rousseaux & Steinling, 1992).

In a spatial attention task autistic patients were not only showing increased reaction times, but they were also less accurate in their reactions than controls (Townsend et al., 1999). Furthermore they profited more from a longer cue to target interval possibly showing a stronger need for time to orient their attention.

However, other studies failed to provide support for the hypothesis that the cerebellum plays a role in attentional processes. Helmuth et al. did not find any differences in a shifting-attention task between cerebellar patients and control subjects (Helmuth, Ivry, & Shimizu, 1997). Ravizza and Ivry showed that reduced motor demands lead to a significant improvement in an alternating attention task in cerebellar patients compared to patients with Parkinson’s disease (Ravizza & Ivry, 2001). Unfortunately in this study no report is given concerning the precise diagnosis of the cerebellar patients or their neurological symptoms. More detailed information here could have contributed to an elucidation of the issue. This is because it would be useful to see whether impairments in patients with degenerative cerebellar diseases are simply due to general cerebellar abnormality, or if the pattern of deficits further depends on the specific diagnosis (i.e. cerebellar infarcts, tumours or degenerative diseases).

Townsend et al. (1999) assume a cerebellar contribution to attention networks, with the cerebellum as an antecedent structure having a relatively unspecific effect on different components. According to this assumption the frontal cortex could only perform its tasks free of limitations on the basis of an unimpaired cerebellar input.

From this point of view the cerebellum is seen as a mechanism predicting internal conditions for a particular motor or mental operation, and then setting the corresponding conditions in preparation. “The cerebellum prepares internal conditions […] by repositioning sensory receptors; by altering cerebral blood flow levels; by enhancing neural signal to noise; by enhancing neural responsiveness in hippocampus, thalamus and superior colliculus; by modulating motor control systems” (Courchesne & Allen, 1997, p. 2). Sensory processing, as well as motor and mental performance, are smoothed and facilitated by these preparations. The cerebellum has to learn the predictive relationships among neural activities in order to prepare internal conditions. A new complex task will lead to strong cerebellar activation, but once a task has been learned cerebellar activity will decrease. The proposed theory predicts that the cerebellum has a relatively global influence on different functions. However, cerebellar damage will not eliminate these functions, but it does increase suboptimal variability in responses and conscious effort when performing motor or mental tasks. The reported difficulties that patients with cerebellar lesions have in shifting their attention in a short cue to target interval may be an example of a reduced, but not eliminated, function. This theory seems to be in accord with the term “dysmetria of thought” postulated by Schmahmann and Sherman (1998). The term dysmetria commonly used for motor impairment in cerebellar patients has been expanded to cognitive functions.

The discussion about the cerebellums’ contribution to attentional processes is still controversial. It is difficult to draw conclusions from studies with autistic patients or patients with degenerative cerebellar diseases because it remains unclear if attentional deficits are only due to cerebellar abnormalities. To improve the understanding of the function of the cerebellum, a study on patients with focal cerebellar lesions is needed. The main goal of our study is to prove whether an undamaged cerebellum is a basic requirement for the optimal functioning of higher cognitive processes and of attention. Deficits should be most pronounced in tasks requiring shifting between different dimensions. Performance in selective attention tasks should also be reduced but not as much as in more complex tasks.

Section snippets

Subjects

Between 2000 and 2002, 16 patients with focal cerebellar lesions (eight male and eight female) were assessed by means of a neuropsychological test battery and then included in a database (Table 1). The age range of the study group was 26–71 years (median: 52 years). Three patients underwent surgery for intracerebellar haematomas and 13 patients for cerebellar tumours (five meningeomas, three metastasis, two haemangiomas, two angiomas, one ganglioglioma). In six patients, the lesion affected the

Results for neuropsychological assessment

Levene’s test for equalitiy of variances revealed that equality of variances between the groups could not be assumed in all tests. Therefore, the Mann-Whitney U-test, a non-parametric test for two independent samples, was used to evaluate statistical significance. Assuming that the cerebellar patients would be impaired, the test was calculated one-sided.

The neuropsychological test battery showed a significantly impaired performance (P<0.05) of the patients in various tests: visual memory

Discussion

This study describes attention deficits in patients with focal cerebellar lesions due to tumour or haematoma.

Clear impairments were seen in divided attention and in working memory. In both tasks misses of target stimuli and false alarms, as well as variance in reaction time, were significantly impaired in the patients (P=0.05). In working memory, the patients proved to be slower in reaction time as well. In the selective attention task (go/nogo), a greater variance of reaction time in the

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