Does the cerebellum contribute to specific aspects of attention?

Neuropsychologia 41 (2003) 1452–1460

Does the cerebellum contribute to specific aspects of attention? Birgit Gottwald∗ , Zoran Mihajlovic, Barbara Wilde, Hubertus Maximilian Mehdorn Department of Neurosurgery, University of Kiel, Universitätsklinikum Schleswig-Holstein, Klinik für Neurochirurgie in Kiel, Weimarer Str. 8, D-24106 Kiel, Germany Received 2 September 2002; received in revised form 12 March 2003; accepted 31 March 2003

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. © 2003 Elsevier Science Ltd. All rights reserved. Keywords: Cognition; Divided attention; Selective attention; Working memory; Cerebellar lesion

1. 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 ∗ Corresponding author. Tel.: +49-431-597-4924; fax: +49-431-597-4884. E-mail address: [email protected] (B. Gottwald).

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.

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B. Gottwald et al. / Neuropsychologia 41 (2003) 1452–1460

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,

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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,

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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. 2. Methods 2.1. 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 left cerebellar hemisphere, and in 10 patients the right hemisphere. The deep cerebellar nuclei were involved, either by tumour or oedema, in 10 cases. In three patients, the vermis was also affected. For organisational reasons it was not possible to see all patients before surgery, and therefore to avoid possible surgical effects. Nine patients were tested as inpatients before surgery, and three after surgery while still in hospital. Four were seen as outpatients 11–27 months after surgery. Ten patients presented a gait ataxia but motor disturbances, as well as dysarthria, were very mild, if existing at all. Pre-operative MRI showed in six cases a slight brainstem compression, in five cases a slight hydrocephalus. The control sample consisted of 16 healthy controls matched for age, gender, and years of education. The age range of the control group was 27–75 years (median: 51 years). Patients and controls gave written consent to participate in this study. 2.2. Neuropsychological assessment Patients and controls received a detailed neuropsychological testing. The following functions were tested: (i) estimation of premorbid intelligence [“Mehrfach Wortwahl test”, MWT-B (Lehrl, 1975)], (ii) memory [Wechsler memory scale-revised, WMS-R (Wechsler, 1987)], (iii) executive functions [semantic and phonematic verbal fluency, five-point test (Regard, Strauss, & Knapp, 1982; Spreen & Strauss, 1998), modified card sorting test, MCST (Nelson, 1976), Stroop-test (Stroop, 1935, for German version see Bäumler, 1985), similarities, WAIS-R (Wechsler, 1981)], (iv) visuo-spatial functions [Rey–Osterrieth complex figure test (Rey, 1941; Spreen & Strauss, 1998)), block design, WAIS-R (Wechsler, 1981)], (v) attention [“Testbatterie zur

Table 1 Patient characteristicsa Patient

Sex

Age in years

Years of education

Diagnosis

Lesion size (cm2 )

Lesion side

Point of assessment

MJ GJ RR MB CH MB PK HS FP ME WJ IG AS RL RH VT

F F F M F F M M M F M F M M F M

50 41 59 37 40 49 61 26 63 54 65 66 36 71 48 45

13 18 11 12 9 18 12 19 10 10 13 11 18 6 12 13

Metastasis Meningeoma Haemangiobl. Angioma Angioma Meningeoma Haematoma Haemangiobl. Haematoma Meningeoma Metastasis Meningeoma Ganglioglioma Metastasis Meningeoma Haematoma

7.5 9 2.25 9 6 22.5 15 1.5 7.5 25 24 27.5 49 6 12.25 3

Left Right Right Left Right Right Right Left Left Left Right Right Right Right Left Right

pre-operation pre-operation 27 months post-operation 26 months post-operation 18 months post-operation pre-operation 11 months post-operation pre-operation post-operation pre-operation pre-operation pre-operation post-operation pre-operation pre-operation post-operation

a

Pre-operation: within 1 week before the operation, post-operation: 1–2 weeks after the operation or number of months.

B. Gottwald et al. / Neuropsychologia 41 (2003) 1452–1460

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Fig. 1. Go/nogo task (presentation of the five possible and the two critical stimuli).

Fig. 2. Divided attention task (example of four crosses forming a square).

Aufmerksamkeitsprüfung”, TAP (Zimmermann & Fimm, 1993), trail-making-test, TMT (Partington & Leiter, 1949; Shallice, 1988)], (vi) motor functions [Purdue Pegboard test (Tiffin, 1968)], (vii) affective state [profile of mood states, POMS (Mc Nair et al., 1981)]. Because this article focuses on attention deficits the attention tasks will be described in more detail.

requires the continuous remembering and comparing of the digits, a task quite difficult for healthy subjects as well. Divided attention: Parallel processing of stimuli of two different modalities is known as a function of divided attention. In the visual part of the task square arrays of crosses are to be recognised. The acoustic part consists of two notes of different pitch presented alternately; subjects are instructed to press the key if they hear the same note twice in a row. (Instruction: “This test consists of two tasks. First task: On the screen you see an area in which various crosses will light up. If four of those crosses form a square please press the response key as quickly as possible (Fig. 2). Second task: In this task you hear alternately a high and a low note. You are asked to detect the presentation of the same note twice in a row. In that case please press the response key as quickly as possible. It is your task to pay attention to the squares and the notes at the same time.”) The two modalities are presented simultaneously, demanding either a very quick shift of attention between the two modalities or parallel attention to both at the same time. Each trial lasts 2000 ms. The notes are presented for 433 ms with an inter-stimulus-interval of 667 ms. In day to day life it is often difficult for patients to do different things at the same time, therefore divided attention tasks are clinically highly relevant. In all three tasks subjects were instructed to respond to targets by pressing the response key as quickly as possible. False alarms and misses were recorded as well as reaction time. The patients’ performance will be compared to the matched control group for all parameters.

2.3. Attention tasks To examine different aspects of attention three computercontrolled sub-tests (“go/nogo”, “working memory”, “divided attention”) of the TAP (Zimmermann & Fimm, 1993) were used. To one patient (RR) only two tests were administered. TAP is a commonly used German attention test battery, including 12 sub-tests. Go/nogo: Five similar patterns were presented in a random order. Two of the five were target stimuli. Subjects were instructed to press the response key as quickly as possible for every presented target stimuli. The three non-target stimuli were to be ignored. (Instruction: “In this test the following patterns will be shown to you in a random order . . . Please press the response key as quickly as possible if you see one of the following patterns . . . ”, Fig. 1.) The stimulus duration is 1000 ms with an inter-stimulus-interval of 2200–3200 ms. Go/nogo is a selective attention task. The demanded response inhibition after non-target stimuli is associated with the prefrontal cortex. Working memory: This task is founded on the assumption that working memory means co-ordinating and re-organising new information by perceiving and processing it. As it is very difficult to separate from attention, working memory can be seen as an attention task in the broader sense. The task is based on the “two-back” principle. Digits are randomly presented. Subjects are instructed to press the response key in those cases where the digit is equal to the last but one. (Instruction: “In this task you will see a random sequence of digits. Sometimes the presented digit is the same as the last but one. In that case please press the response key as quickly as possible.”) The inter-stimulus-interval is 3000 ms, the stimulus duration time 1500 ms. This task

3. Results 3.1. 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

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Table 2 Results of the neuropsychological assessment for patients and controlsa Test

Mean

S.D.

Patients Premorbid intelligence

MWT-B#

68.91

Memory

Verbal memory (WMS-R)◦ Figural memory (WMS-R)◦

99.80 89.75

Executive functions

Verbal fluency Semantic# Phonematic∗

19.73 46.10

Five-point test Number of drawings# Percent of perseveration#

24.38 8.13

MCST Number of categories#

Visuo-spatial functions

Attention

Controls

6

P

Patients

Controls

85.04

30.70

15.51

n.s.

113.38 110.13

26.86 22.10

13.41 11.7

n.s. 0.003

26.53 82.50

4.46 36.02

7.19 24.77

0.005 0.002

30.50 7.35

13.09 9.59

8.47 6.01

n.s. n.s.

0

n.s.

6

0

Stroop test Word reading∗ Colour naming∗ Interference∗ Similarities (WAIS-R)+

47.00 46.80 53.07 9.88

69.81 68.19 68.50 12.88

23.62 21.36 20.98 3.63

27.26 24.61 25.89 2.13

Rey–Osterrieth figure Copy# Recall# Block design (WAIS-R)+

32.33 14.80 9.47

33.75 17.06 11.25

2.94 6.46 3.23

2.03 7.61 3.19

Trail-making-test Part A∗ Part B∗ Part B–Part A∗

39.87 47.91 47.03

69.53 73.22 70.31

26.91 26.92 33.11

19.76 19.92 25.30

0.002 0.003 0.028

2.94

1.59

0.019

7.13 11.19 26.38 3.81

8.62 6.28 5.90 6.64

0.003 0.039 0.000 n.s.

Motor function

Purdue Pegboard (both hands)#

Affective state

POMS Dejection# Tiredness# Initiative# Discontent#

8.73

11

22.73 15.73 16.00 5.53

18.87 8.11 6.64 10.03

n.s.: not significant, ∗ : percentiles, # : raw score, ◦ : indices (mean = 100, S.D. = 15), a P: significance after one-tailed Mann-Whitney U-test.

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 (WMS-R), word fluency, Stroop-test, similarities (WAIS-R), trail-making-test (Part A, Part B, B–A) and Purdue Pegboard. Rating their affective state in the profile of mood states, they saw themselves as reduced in initiative and very dejected and tired (Table 2). 3.2. Results for attention tasks The comparison of the raw data led to the following results. In the go/nogo task, patients showed a slightly greater variance of reaction time compared to the controls (S.D. of reaction time: U = 89.0, P = 0.075). There were no sig-

+:

0.009 0.010 0.023 0.008 n.s. n.s. n.s.

scaled score (mean = 10, S.D. = 3).

nificant group differences in the median of reaction time or in false alarms and misses (Table 3). The working memory task showed significant deficits of the patients compared to the controls, both for the reaction time parameters and for misses and false alarms (S.D. of reaction time: U = 77.0, P = 0.047; median of reaction time: U = 75.0, P = 0.039; misses: U = 78.5, P = 0.050; false alarms: U = 77.5, P = 0.047). One patient (RL) performed randomly in this task (46 false alarms). For the calculations of mean and S.D. (Table 3) his results have not been taken into account. Pronounced differences were shown in divided attention. Although patients were not slower in reaction time than controls, the qualitative performance was clearly impaired. They missed a significant amount of target stimuli (misses: U = 61.5, P = 0.006) and responded at the same time to more non-targets (false alarms: U = 78.5, P = 0.031). Variance in reaction time was also larger in patients than

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Table 3 Results of the attention task parameters (S.D. and mean in milliseconds, numbers of misses and false alarms) for patients and controlsa Test

Mean

S.D.

Patients

Controls

Go/nogo S.D. Median Misses False alarms

96.88 591.16 1.19 2.5

Working memory S.D. Median Misses False alarms Divided attention S.D. Median Misses False alarms

Mean percentiles

Patients

Controls

81.67 563.25 0.50 3.56

33.63 95.95 2.46 4.32

266.95 734.93 4.07 4.57

184.50 632.94 2.06 2.44

261.95 713.00 4.2 3.07

215.97 692.50 1.69 1.75

P

Patients

Controls

35.35 98.99 1.75 11.37

34.25 38.00 – 33.75

55.69 48.81 – 39.88

0.075 n.s. n.s. n.s.

141.06 183.06 3.10 4.40

93.90 213.77 1.61 2.34

30.93 25.93 21.87 33.80

49.19 48.06 33.65 52.50

0.047 0.039 0.050 0.047

81.82 100.28 3.84 2.91

69.82 66.03 1.96 2.27

38.44 26.94 21.31 –

56.81 31.56 49.62 –

0.031 n.s. 0.006 0.031

n.s.: not significant, –: no normative data available. Two patients were excluded in one task each because of performance at chance. RL: working memory, AS: divided attention. a P: significance after one-tailed Mann-Whitney U-test.

in controls (U = 78.0, P = 0.031). One patient performed randomly in this task (AS, 44 false alarms). His results have not been taken into account for the calculations of mean and S.D. (Table 3).

To illustrate the differences, Fig. 3 shows the results in percentiles, based on normative data of the TAP (normative data for misses in go/nogo and false alarms in divided attention do not exist).

Fig. 3. Mean percentiles of median (Md) and standard deviation (S.D.) of reaction time (RT), misses and false alarms (False A) of divided attention (Divided A), working memory (Working M) and go/nogo in cerebellar patients and controls. ∗ P < 0.1, ∗∗ P < 0.05 after one-tailed Mann-Whitney U-Test.

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Table 4 Clinical data and attention deficits Patient

Aetiology

Lesion size (cm2 )

Lesion side

Divided attention

Working memory

Go/nogo

MJ GJ RR MB CH MB PK HS FP ME WJ IG AS RL RH VT

Metastasis Meningeoma Haemangiobl. Angioma Angioma Meningeoma Haematoma Haemangiobl. Haematoma Meningeoma Metastasis Meningeoma Ganglioglioma Metastasis Meningeoma Haematoma

7.5 9 2.25 9 6 22.5 15 1.5 7.5 25 24 27.5 49 6 12.25 3

Left Right Right Left Right Right Right Left Left Left Right Right Right Right Left Right

o o x o o o x o x x x o x x o x

o x – o x x x o x x x x x x o x

o o x o o o o o o o x x x x o o

x: deficit (percentile <16), o: no deficit, –: not tested.

Three patients have been tested post-operatively as inpatients. Their performance may have been additionally reduced by direct post-operational consequences. To check possible influences, the data has been analysed without these three patients to see if results change. This reduction of the sample to only 13 patients and 13 controls did indeed reduce the differences. The slightly greater variance in go/nogo was not significant anymore (P = 0.11) neither was the difference of misses in working memory (P = 0.135). In other test parameters, only slight differences were discernible (P < 0.1: variance in working memory and in divided attention). Significant differences remained in misses and false alarms in divided attention, and in median of reaction time and false alarms in working memory (P < 0.05). Possible relations between diagnosis, size, laterality of tumour or haematoma and attention deficits are looked at descriptively (Table 4). Lesion size is measured in cm2 in pre-operative MRI. It is defined by the largest and second largest tumour extension in two different dimensions out of the horizontal, sagittal and coronar dimensions. There seems to be no relation in the data between lesion size and attention deficits. There is no direct correlation discernible between diagnosis and attention. Attention performance has not been influenced by whether the disease had a sudden onset or not. There is no definite relation between laterality of the lesion and attention. The fact is, however, that the four patients who had no deficits in either of the attention tasks had left-sided lesions, whereas all patients with right-sided lesions showed difficulties in at least one of the tasks. Although all patients suffered from focal cerebellar lesions, the anatomical proximity to the brainstem needs to be taken into account if there has been a pre-operative brainstem affection. This is because of the possible consequences on the intensity of attention. In 5 of the 16 patients, a slight suppression could not be excluded. However, a direct correlation to attention deficits could not be proved either.

A pre-operatively existent hydrocephalus can lead to global impairments because of the increase of pressure. MRI showed a slight pre-operative hydrocephalus in 5 of the 16 cases. But again, to see this as the only reason for the attention deficits is out of the question. Firstly, this is because attention deficits were also seen in patients without any sign of hydrocephalus, secondly hydrocephalus leads typically to mental slowing and memory impairment (Lezak, 1995) which were not found in the corresponding patients.

4. 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 patients was the only slightly significant difference. Courchesne and Allen (1997) describe in their theory a global preparation role of the cerebellum. In simplified terms, the cerebellum prepares the way for expected stimuli, optimising their processing and readiness for reaction. Cerebellar damage should therefore not eliminate functions but instead impair the performance. Demands on such a preparation system should be especially high if a rapid shift between two modalities, or their parallel processing, is required. The divided attention task that was used is such a task. These high demands led to many misses of targets and many false alarms in the patients. In the quite difficult working memory task, the patients showed an impaired performance in every parameter. Except

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for one patient, they were all able to perform the task; the function was not eliminated but reduced. This reduction may be due to a deficit of the central executive—one aspect of working memory. The central executive not only contributes to the maintenance and manipulation of items in working memory, but is also involved in many other tasks demanding prediction and preparation, and seems therefore comparable to the described predicting function of the cerebellum. In all three tasks, the patients showed a higher variability in reaction time than the controls, indicating an uneven and not very smooth task performance. Except for the higher variance, no impairment was seen in the selective attention task (go/nogo), the easiest of the three tasks. This task demands no switching between modalities or parallel processing, therefore the impairment of the preparing mechanism might not have had as many consequences. The fact that most of the differences remained significant after the three post-operatively tested patients (and their matched controls) had been excluded, shows that direct post-operative effects have only had an additional effect to those deficits due to cerebellar lesion. In the attention tasks the demanded response consisted of pressing a response key with the preferred hand. Motor impairments should have been seen, if existent, in all three tasks, manifesting themselves in slowed reaction times. This was not the case. Working memory was the only task showing longer reaction times in patients than in controls. In go/nogo, the task requiring the shortest reaction time, there was no difference between patients and controls. In addition the disturbances in qualitative aspects (misses and false alarms) cannot be explained by motor impairment either. The neuropsychological battery showed significant impairments of the patients compared to the controls in verbal fluency tasks, in finding verbal similarities (WAIS-R: similarities), in the Stroop test, and in figural memory. Although patients showed motor deficits as well (Purdue Pegboard), this cannot explain the cognitive impairment. TMT performance was below average in Parts A and B, but the difference between both parts (A–B) known as complex—double or multiple—conceptual tracking (Lezak, 1995) was significantly impaired in the patients. On top of that, impairments were not limited to speed tests, but were recorded in tests without a time limit as well (WAIS-R: similarities, figural memory). Deficits in tasks normally associated with frontal lesions, such as verbal fluency and similarities, have also been proved by Schmahmann and Sherman (1998). However, no memory deficits have been reported by those authorities. Compared to the controls the patients felt very dejected, tired and reduced in initiative. The question remains open as to whether these changes in mood are due to cerebellar lesions, or just a reaction to knowledge of their diagnosis or the fact that they were in hospital. All cerebellar patients suffered from focal cerebellar lesions. The motor disturbances, as well as dysarthria, of all the patients were very mild, if existing at all. Viewing

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pre-operative MRI, a slight hydrocephalus or suppression of the brainstem could not be excluded in a few patients. However, a direct effect on cognitive functions did not exist, especially given that after hydrocephalus a general slowing down of the patients would be expected, something not seen in this sample. Aetiology did not seem to have had direct consequences on cognitive performance, nor did the lesion size. Comparing patients with right- and left-sided lesions it is obvious that all those without any attention deficits had a left-sided lesion. Patients with right-sided lesions seem to have had more deficits altogether. This fact is surprising given that attention functions are usually associated with the right cerebral hemisphere, corresponding to the left side of the cerebellum according to the crossed cerebro-cerebellar connections. Which cerebellar hemisphere is dominant for attentional processes has not been definitely established. Location of cerebellar activation shown by fMRI seems rather dependent on the specific attention task (Allen et al., 1997; Le et al., 1998). Deficits in divided attention after right cerebellar lesions are in accordance with reported right-sided activation in a shifting-attention task (Le et al., 1998). When looking at cerebro-cerebellar diaschisis another explanation seems possible: necessary inhibition processes in attention tasks are reported to activate left frontal regions (Stroop, 1935). In our study, reduced inhibitory processes were manifested by the many false alarms produced by cerebellar patients in the divided attention and the working memory task. This was especially pronounced in patients with right cerebellar lesions. There is a very strong connection between higher attentional processes and executive functions such as inhibition processes, which are also located in frontal areas. Additional executive deficits should therefore intensify attentional problems. Our results confirm that attention deficits, and other cognitive deficits, occur after focal cerebellar lesions. The pronounced poor results of the patients in divided attention are of great clinical importance because they are relevant functions for daily life. The assumption of Courchesne and Allen (1997) that deficits in the predictive function of the cerebellum after cerebellar lesions lead to sub-optimal performance, is supported by the results. These deficits were seen most clearly in the divided attention and the working memory task. The question of whether the right cerebellar hemisphere is more involved than the left in attentional processes requires further investigations.

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