Absence of a common functional denominator of visual disturbances in cerebellar disease

Brain (1999), 122, 2133–2146 Absence of a common functional denominator of visual disturbances in cerebellar disease Peter Thier,1 Thomas Haarmeier,1 Stefan Treue1 and Shabtai Barash2 1Sektion für Visuelle Sensomotorik, Neurologische Universitätsklinik Tübingen, Germany and 2The Weizmann Institute, Rehovot, Israel Correspondence to: Professor Dr P. Thier, Sektion für Visuelle Sensomotorik, Neurologische Universitätsklinik, Hoppe-Seyler-Straße 3, 72076 Tübingen, Germany E-mail: Summary Several studies have demonstrated disturbances of visual perception in patients suffering from cerebellar disease. In an attempt to determine the cause of these visual disturbances and thereby the cerebellar contribution to vision, we designed two sets of experiments in which we tested (i) the possibility of a general magnocellular deficit in cerebellar disease and (ii) the alternative possibility of impaired spatial attention underlying visual disturbances in cerebellar patients. The first set of experiments consisted of a test of position discrimination, a parvocellular function and tests tapping different aspects of motion perception including speed discrimination, direction discrimination and the ability to extract a coherent motion signal embedded in noise. The second set of experiments compared the performance on two different classes of texture discrimination. The first one required fast and precise shifts of focal spatial attention (‘serial search’), the second one, testing preattentive texture discrimination (‘pop-out’), did not. In the first set of experiments cerebellar patients were impaired on the position discrimination task as well as several, albeit not all, tests of motion perception. The pattern of disturbances obtained was neither compatible with the notion of a selective magnocellular deficit nor the idea, originally put forward by Ivry and Diener (J Cogn Neurosci 1991; 3: 355–66) that visual deficits are secondary to an impaired measurement of time. In the second set of experiments, cerebellar patients showed normal performance on popout tasks and normal performance on all variants of the serial search task except for the one requiring comparison of a single element presented with a sample of the target in short-term memory. In summary, our results support the existence of visual disturbances in cerebellar disease, but provide evidence against a common, simple denominator such as a timing deficit, deficient cerebellar modulation of magnocellular circuitry, deficits of spatial attention or visual working memory. Keywords: visual motion; memory; attention; clock; timing; cerebellum Abbreviations: ANOVA 5 analysis of variance; RDP 5 random dot patterns; SOA 5 stimulus onset asynchrony Introduction Recent years have witnessed a dramatic change of our view of the vertebrate cerebellum. While the cerebellum has traditionally been viewed as a brain centre subserving skilled motor behaviour, recent work on the human cerebellum has suggested a much broader functional role with contributions to a wide range of cognitive functions including visual perception (Fiez, 1996). The view that the cerebellum is involved in visual perception goes back to work undertaken on cerebellar patients by Ivry and Diener (Ivry and Diener, 1991). These authors reported that their patients, most of them suffering from degenerative cerebellar disease, were impaired on tasks requiring the discrimination of the speeds of sequentially presented patterns. The same patients were normal on a task demanding the discrimination of two simultaneously presented positions in different parts of the © Oxford University Press 1999 visual field. Recoursing to the physical definition of velocity as a position increment divided by a time increment, and having demonstrated a normal capability of sensing position increments in the face of an impaired capability to measure velocity, these authors concluded that this impairment in speed discrimination was a consequence of an impaired capability to measure time increments. This specific interpretation seemed to add support to the idea that the cerebellum is a biological clock measuring time intervals in the milliseconds range subserving motor as well as nonmotor functions (Keele and Ivry, 1990). Irrespective of this very specific interpretation, the existence of a motion perception deficit received further support when Nawrot and Rizzo demonstrated that cerebellar patients were impaired on a task requiring the extraction of a coherent motion 2134 P. Thier et al. signal embedded in noise (Nawrot and Rizzo, 1995). Their experiments were designed to account for the two major objections raised against the Ivry and Diener study. The first one is that the perceptual deficits seen might have been due to an involvement of extracerebellar structures, often affected by genetically determined cerebellar disease. The second objection usually put forward is that visual disturbances might have been a consequence of subtle oculomotor disturbances such as instability of fixation during stimulus presentation. Therefore, Nawrot and Rizzo restricted stimulus presentation to 200 ms, thereby reducing the impact of possible instabilities of fixation, and they studied patients with vermal lesions of non-degenerative cause, thereby excluding the possible impact of extracerebellar pathology. While their well-controlled study has clearly strengthened the case for motion perception deficits resulting from a true cerebellar dysfunction not being secondary to oculomotor disturbances, it has not been able to unravel its cause. A possible cause of motion deficits is suggested by previous work on the visual cortex of cats. It has been known for many years that the motion processing areas of the cat, the suprasylvian sulcus, receive a strong input from those parts of the thalamus which are under cerebellar control (Sasaki et al., 1972; Wannier et al., 1992), suggesting some kind of modulatory influence of the cerebellum on motion processing. Primate cortical areas such as MT and MST, often assumed to be homologous to the suprasylvian motion processing areas of the cat, are the major targets of an anatomically and functionally distinct pathway fed by the magnocellular part of the lateral geniculate body (Merigan et al., 1991; Maunsell, 1992). These facts in mind, we wondered if motion perception deficits in cerebellar patients might actually reflect a missing or reduced cerebellar influence on the magnocellular pathway. In this case one would expect to find impairments of all magnocellular visual functions, not only the time dependent ones such as the ability to discriminate speeds. We set out to test this idea as an alternative to the timing deficit hypothesis of Ivry and Diener by comparing cerebellar patients with healthy controls on a battery of paradigms (Study 1) tapping different aspects of motion perception including tests of speed discrimination, direction discrimination and th (...truncated)