The size-weight illusion, emulation, and the cerebellum

In this commentary we discuss a predictive sensorimotor illusion, the size-weight illusion, in which the smaller of two objects of equal weight is perceived as heavier. We suggest that Grush’s emulation theory can explain this illusion as a mismatch between predicted and actual sensorimotor feedback, and present preliminary data suggesting that the cerebellum may be critical for implementing the emulator. If a person compares the weight of a large object with that of a small object of identical physical weight, the latter will feel substantially heavier, even though the person is explicitly asked to compare the weight rather than the density. This effect – the socalled “size-weight illusion” – is a striking demonstration of the principle that perception is predictive and does not simply involve a passive response to sensory inputs (Charpentier 1891; Ross & Gregory 1970). Traditionally, it has been suggested that the brain expects the bigger object to be much heavier and sets the muscle tension accordingly, and so when the larger object is lifted it feels surprisingly light (Ross 1966; Ross & Gregory 1970), indeed lighter than a small object of identical weight. However, recent evidence has shown that the size-weight illusion (SWI) persists despite adaptation of these peripheral lifting movements (Flanagan & Beltzner 2000), suggesting that the source of the illusion may be a central mismatch between the expected and actual sensory feedback. We therefore suggest that the source of the mismatch in the SWI may be an internal sensory prediction, which, after a lifetime of experience, generates an erroneous weight prediction, yielding a sensory residual and the corresponding illusion (Hubbard et al. 2000; in preparation). One prediction that we made on the basis of this hypothesis is that patients with damage to the cerebellum, which has been implicated in weight perception (see Holmes 1917; 1922), may also show reductions in the SWI, even in the absence of impairments in weight perception. A number of researchers (e.g., Kawato 1990; Wolpert et al. 1995; and Grush in the present target article) have suggested that predicting the sensory consequences of motor actions may be a function of portions of the cerebellum, especially the dentate nucleus. These speculations led us to wonder whether the cerebellum may be involved not only in overt movement, but also in cognitive simulation prior to movement, functioning as a “Grush emulator” (Grush 1995; target article), or forward model (Jordan & Rumelhart 1992). This line of reasoning is also supported by the observation that neurons in the lateral cerebellar cortex (specifically lobules V and VI) respond to the anticipated sensory consequences of an action (Miall 1998). To test this prediction, we tested six control subjects and seven cerebellar patients. Cerebellar patients of varying etiologies were referred to us by physicians on the basis of neurological assessment. Patients showed typical signs of cerebellar dysfunction including intention tremor, past pointing, and dysdiadochokinesia. To assess weight discrimination, subjects were presented with a pair of weights differing in weight by 50 grams and were asked to state which of the two cans was heavier. We used both a pair of large cans (300 g, 350 g) and a pair of small cans (150 g, 200 g). Each subject was tested twice. After assessing weight discrimination, we assessed the magnitude of the SWI by asking subjects to determine which of 10 small cans (ranging from 100–275 g) matched the apparent weight of the large 300-gram can. Each subject was tested four times. The six control subjects showed accurate weight discrimination. Subjects made errors on a total of four out of 24 trials, and no subject made more than one error. However, when asked to match the weight of the large 300-gram can, control subjects showed a clear SWI, matching the large can with a can that weighed substantially less (mean 151.04 g). The magnitude of the illusion is far greater than the minimum difference that can be discriminated – the illusion is not due to an inability to discriminate the weight of the cans. On the other hand, five of seven cerebellar patients showed a reduction of the SWI, despite intact weight discrimination. The first patient, a middle-aged woman showing acute unilateral cerebellar signs (left hand) caused by secondary tumor metastasis in the brain, showed the most dramatic effect. She was mentally lucid, intelligent, and articulate. She showed cerebellar signs – intention tremor, past pointing, and dysdiadochokinesia – only in the left hand. Her ability to estimate subtle differences in weight was identical in both hands. However, the left hand showed no SWI, whereas the right hand showed the illusion in full strength. She expressed considerable surprise that the two hands were producing different results on the task. There was some recovery from cerebellar signs on the following day, and this time the left hand showed the illusion, but still it was substantially smaller than in the normal, right hand. The subsequent six patients had bilateral cerebellar damage caused by injury, infarction, and electrocution (one patient). Unlike the first patient, they were seen weeks to months after the onCommentary/Grush: The emulation theory of representation: Motor control, imagery, and perception BEHAVIORAL AND BRAIN SCIENCES (2004) 27:3 407 set of the lesion. Two of these showed the full SWI, despite florid bilateral cerebellar signs. The other four showed a small reduction of the illusion (mean 175 g in the four patients who showed the effect, with almost 210 g in one of them, compared to the 300 g standard). These experiments provide some preliminary evidence that the cerebellum may be involved in sensory predictions of overt motor behavior and thereby contributes to the SWI. However, these results are not conclusive. Future research should be conducted with additional cerebellar patients to distinguish between three hypotheses: (1) a specific part of the cerebellum serves as a Grush emulator and this was severely damaged in Patient One but less damaged in the others; (2) Patient One may have had some other metastatic lesion causing the reduction of the SWI, for example, a zone in the basal ganglia or frontal lobes that receives information from the cerebellum rather than in the cerebellum itself; or (3) the loss of the SWI may be seen only acutely (as in Patient One) and, given the cerebellum’s remarkable adaptive capacities, may have recovered substantially in the other patients. These findings suggest that the cerebellum may be involved in perceptual and cognitive predictions, functioning as a Grush emulator or forward model for internal simulations before performing certain tasks. The role of “prespecification” in an embodied cognition