We and others have shown that individuals with cerebellar damage are impaired at recalibrating the relationship between gaze and throw direction when a prismatic perturbation is introduced. While prism adaptation can affect vision and proprioception as well as motor commands, we used the task paradigm described by Martin et al. (1996b)
, who showed that the pattern of generalization from this task is inconsistent with visual or proprioceptive recalibration. The authors concluded that the adaptation was mostly motor (Martin et al. 1996b
), thus we interpret the cerebellar impairment in prism adaptation in the present study as a deficit in motor adaptation. Within the same subjects, we find intact ability to perform visuoproprioceptive realignment similarly to healthy controls in a reaching task: impairment was seen only when motor adaptation was possible in addition to sensory realignment. This suggests that unlike motor adaptation, sensory realignment is not a cerebellum-dependent process.
Motor adaptation is a well-studied phenomenon. When a mismatch is detected between the predicted and actual sensory outcome of a motor command, the command is adjusted accordingly (e.g., Tseng et al., 2007
). Storage of a new relationship between motor command and sensory outcome is assessed by looking for an aftereffect, and is the only robust test of whether motor adaptation has occurred. This is because cerebellar patients are known to be able to use a conscious aiming strategy to reduce error during adaptation, which does not lead to storage of a new motor command (Taylor and Ivry, 2011
). Cerebellum-dependent motor adaptation has been found in reaching (e.g., Weiner et al., 1983
; Baizer et al., 1999
; Tseng et al., 2007
), walking (Morton and Bastian, 2006
), and throwing (Martin et al., 1996a
). When a visuomotor perturbation is introduced in a throwing task by placing prisms over the subject’s eyes, for example, cerebellar patients do not recalibrate gaze direction and throw direction as much as controls do (Martin et al., 1996a
), a finding we confirmed in Experiment 1 of the present study.
However, the cerebellum has been linked to sensory as well as motor processing. Gao et al. (1996)
found, by imaging of the dentate nucleus, that the lateral cerebellum is activated by the acquisition and discrimination of sensory information. In a study of illusory hand flexion with congruent or incongruent visual feedback, Hagura et al. (2008) determined that activity in the posterolateral cerebellum was correlated with the subjective sensory perception of hand movement, suggesting that this region of the cerebellum is involved in multisensory processing. Indeed, it has been proposed that the lateral cerebellar zones are involved exclusively in sensory processing and not motor control (Parsons et al., 1997
). Synofzik et al. (2008)
found that patients with cerebellar lesions were impaired at predicting visual consequences of movement and suggest that the cerebellum is important for perceptual learning.
We therefore wondered if the cerebellum might be important for sensory realignment, when the spatial relationship between different sensory estimates is changed (e.g., the proprioceptive estimate of hand position may be realigned to more closely match the visual estimate or vice versa; van Beers et al., 2002
). The cerebellum receives information from virtually every sensory modality (Brodal, 1978
), including vision (Snider and Stowell, 1944
; Glickstein, 2000
) and proprioception (Bauswein et al., 1983
; Donga and Dessem, 1993
), so it is conceivable that different sensory estimates could be compared by the cerebellum. Further, characteristics of the complex spikes carried to cerebellar cortex by olivary climbing fibers (reviewed by Ito, 2001
) make them possible candidates for an error signal arising from any mismatch between sensory modalities. The cerebellum also receives projections from premotor and association areas of cortex, such as posterior parietal cortex (Brodal, 1978
) and projects to motor and premotor areas. Thus, other brain regions that are concerned with the spatial relationships among sensory modalities could theoretically have access to information processed by cerebellar circuits.
In the Sensorimotor experiment (reaching with endpoint visual feedback), we found that patients with bilateral cerebellar ataxia weighted vision and proprioception similarly to controls, suggesting that sensory weighting, at least, is not a cerebellum-dependent process. As a misalignment between visual and proprioceptive estimates of target hand position was gradually imposed, patients and controls both changed the extent of their reaches to unimodal proprioceptive targets in the direction of the perturbation, suggesting some adaptive process was at work. However, the effect was significantly smaller in patients than controls. We have previously found that in controls, the change in reach endpoints for P targets in the Sensorimotor experiment reflects both motor adaptation of the reaching hand and sensory realignment affecting the target hand. The former was presumably driven by the explicit error signal provided by endpoint visual feedback, and the latter by the mismatch imposed between visual and proprioceptive estimates of target hand position (Block and Bastian, 2011
). Given that cerebellar patients are impaired at motor adaptation (Motor experiment, throwing with prisms), we speculated that the change in P endpoints for patients in the Sensorimotor experiment reflects mostly sensory realignment. In other words, the patients had a smaller change in P endpoints than controls because they had the sensory realignment component but largely lacked the cerebellum-dependent motor adaptation component exhibited by controls.
A reasonable question is whether the difference could instead be due to the dissimilarity of the two tasks: the perturbation was gradual in the Sensorimotor experiment (reaching with endpoint visual feedback), but sudden in the Motor experiment (throwing with prisms). This raises the possibility that cerebellar patients shifted their P endpoints in the Sensorimotor experiment because the gradual perturbation was less difficult or less cerebellum-dependent, and not because they were using sensory realignment rather than motor adaptation. Criscimagna-Hemminger et al. (2010) found that cerebellar patients were less impaired at force field learning when the perturbation was gradual as opposed to abrupt. It is possible that the adaptation exhibited by cerebellar patients in the Sensorimotor experiment had both sensory and motor components, but regardless, they adapted significantly less than healthy controls, and the Sensory experiment suggests their deficit is not in sensory realignment. Also, Robertson and Miall (1999)
have shown by reversibly inactivating monkey dentate that the cerebellum is just as crucial for gradual visuomotor adaptation, a task more similar to the present study, as for sudden, if not more so. It therefore seems unlikely that the difference in perturbation can account for the differences in patient performance between the Motor and Sensorimotor experiments.
Another question to consider is whether patients were impaired in the Sensorimotor experiment because they had difficulty using the visual error feedback, which was not present in the Sensory experiment, rather than because they were impaired at motor adaptation. Data from the Motor experiment suggests that the patients in this study did not have difficulty responding to visual error feedback, however. The patients changed their behavior to throw closer to the target when wearing prisms. The prism literature (e.g., Welch 1986) indicates that when people adapt to prisms, some amount of cognitive correction for visual errors can occur on top of the visuomotor adaptation. This is why negative aftereffects are the only “proof” that visuomotor adaptation (and not just a cognitive correction strategy) has occurred. Given that their negative aftereffects were small, the cerebellar patients in the Motor experiment appear to have been relying heavily on such cognitive strategies during adaptation (i.e., using the visual feedback to make corrections), consistent with a recent report by Taylor and Ivry (2011)
. The fact that patients could use this type cognitive strategy with prisms, even though they did not learn and store the new calibration, suggests that they do not have difficulty responding to visual error feedback.
The results of the Sensory experiment (reaching without endpoint visual feedback) demonstrate that, in the context tested here, cerebellar patients are unimpaired at sensory realignment. Recall that the Sensory experiment was identical to the Sensorimotor experiment, except no endpoint visual feedback was given, so the explicit error signal needed to drive motor adaptation was absent, and any shift in P endpoints can be interpreted as a change in the proprioceptive estimate of target hand position, i.e., sensory realignment (Block and Bastian, 2011
). In this situation, patients shifted P endpoints just as much as controls did, suggesting that sensory realignment is not dependent on the cerebellum.
Further support of this comes from the lack of correlation between prism adaptation negative aftereffect (Motor experiment) and the shifting of proprioceptive target endpoints (Sensorimotor and Sensory experiments). i.e., the patients who were least impaired at prism adaptation were not the ones who exhibited the greatest shift in proprioceptive target endpoints during reaching. The lack of correlation suggests that in the Sensorimotor and Sensory experiments, cerebellar patients relied primarily on a process that is not cerebellum-dependent; i.e., sensory realignment.
Given the lesions of the patients we tested, we can speculate that sensory realignment requires neither the cerebellar cortex nor the deep cerebellar nuclei, nucleo-olivary pathway, nor dentate-to-thalamocortical pathways. We propose that sensory realignment may depend instead on regions within posterior parietal cortex (PPC). Many regions within PPC are multimodal; that is, they respond to more than one sensory modality. This multimodal quality is widely thought to be the basis for sensory integration (e.g., Grefkes and Fink 2005
). Additionally, a neuroimaging study by Clower et al. (1996)
suggested that activity in a region of PPC could represent proprioceptive realignment in response to continual prism perturbations. This activity was located in an area within PPC along the intraparietal sulcus in the angular gyrus.
In sum, we have shown that cerebellar patients with motor adaptation impairments do not have sensory realignment deficits. This suggests that unlike motor adaptation, sensory realignment is not cerebellum-dependent. These results have implications for our understanding of sensorimotor processing as well as the capacity for adaptation of individuals with cerebellar damage. That sensory realignment and motor adaptation rely on different neural substrates raises interesting questions for future study. It seems likely that the two processes may operate at the same time in any sensorimotor task where a sensory misalignment occurs and explicit error feedback is available, as in the Sensorimotor experiment. Sensory weightings also appear to operate in support of hitting the target in this situation (Block and Bastian, 2011
). If the neural bases of all three processes can be found, the mechanisms and relationships among them may be better clarified, which could help answer fundamental questions about how sensory and motor processes interact when the brain is confronted with a sensory perturbation, and also provide direction in rehabilitation of patient groups with sensorimotor deficits.