To move the tip of the thumb accurately requires knowledge not only of relative muscle lengths and joint angles (for review see McCloskey, 1978; Gandevia, 1996), but also information about the dimensions of body segments. Indeed, without knowledge of the size of body segments, information related to joint angles is unable to specify uniquely the location of an extremity in space. Skill in normal movements, especially those involving the hand, presumably relies on sensory information received by cortical somatosensory areas before and during the movements (Porter & Lemon, 1993). However, in adult non-human primates and other experimental animals, cortical ‘representations’ of the digits are not fixed but change when amputation or anaesthesia removes the sensory input from them. This adaptation has a rapid phase beginning within minutes (Kelahan & Doetsch, 1984; Calford & Tweedale, 1988, 1991a) and a longer phase developing over weeks and months (e.g. Merzenich et al. 1983, 1984; see also Rasmusson et al. 1992; Zarzecki et al. 1993; for review see Kaas, 1991). Initially, in both flying foxes and monkeys, cells in the primary somatosensory cortex which represent the ‘lost’ digit respond to a larger area of cutaneous input, including that from more proximal skin and even skin on the adjacent fingers (Calford & Tweedale, 1988, 1991a). Acute changes may also occur at thalamic (Rasmusson et al. 1993) and possibly at cuneate levels (Dostrovsky et al. 1976; Pettit & Schwark, 1993; Northgrave & Rasmusson, 1996). Studies in human subjects have also revealed that the behaviour of the sensorimotor cortex is also not fixed. Human motor cortical ‘maps’ assessed with transcranial magnetic stimulation change acutely with local anaesthesia (Brasil-Neto et al. 1993; Kew et al. 1994). These studies have focused on apparent changes to motor and sensory representations produced by local anaesthesia, nerve section or amputation, but the perceptual implications of the altered sensory inputs have rarely been considered.
Some recent studies have indicated the extent to which sensory maps may change under extreme circumstances. When sensory input from the whole arm was removed years previously by an extensive dorsal rhizotomy in monkeys, the cortical representations of the hand and face reorganized over years with the areas usually devoted to the arm map being ‘invaded’ by inputs derived from the chin (Pons et al. 1991). After long-standing amputation of the hand, some patients sometimes mistakenly localize stimuli on the face to the ‘phantom’ hand (Ramachandran et al. 1992; Halligan et al. 1993), a phenomenon which has been taken, along with other evidence, to indicate the potential reorganization of the human somatosensory cortex following nerve injury (see Yang et al. 1994; Elbert et al. 1994). However, the subjective responses to stimulation of cutaneous nerve fascicles innervating the hand are preserved after amputation (Schady et al. 1994).
The present studies were designed to determine whether perceptual disturbances develop when the afferent input from a body part, usually the thumb, is acutely disturbed. Disturbances included both acute decreases in input produced by local anaesthesia and increases produced by innocuous electrical stimulation or painful cooling of the digits. We devised simple psychophysical techniques (selection by the subject of matching templates of body parts, and drawing by the subject of body parts to depict their size) and showed that the perceived size of a body part can change immediately its sensory input is altered. Some results have been published in abstract form (Gandevia, 1994; Glasby & Gandevia, 1995)
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The thumb appeared to grow in size following complete anaesthesia of its digital nerves (Figs 2 and 3). Within seconds of anaesthesia, many subjects spontaneously reported that the thumb felt larger. There was no discomfort reported for the thumb and no evidence that anaesthesia had developed outside the territory of the thumb's digital nerves. Based on subjects’ reports and their drawings it seems that the whole thumb is perceived to grow. The effect was not restricted to the proximal or distal part and involved an increase in the thumb's length and width. The illusion of enlarged size did not require the subject to view the thumb or to touch it with sentient parts of the body - such strategies were minimized by the methods used. The ‘growth’ of the thumb was documented with two methods, template matching and line drawing. Different groups of subjects were used for these two studies. As this illusion occurred when subjects drew around the hand (Figs 2B and 3), the motor system must take account of the changes in perceived body size evoked by thumb anaesthesia. With both methods of measurement, the mean increase in perceived area of the thumb was about 60-70 %. The changes were statistically significant for both groups of subjects (P < 0.001) and for most individual subjects. In no subject did perceived size of the thumb decrease when it was anaesthetized. In a control study using the usual template method, injection of the same volume of saline as for the digital nerve blocks produced no change in perceived size of the thumb.
When the subjects drew an outline of the hand and its digits during thumb anaesthesia, we examined whether there were perceptual changes involving the whole hand and individual digits. The most obvious change in the drawings was the increase in size of the thumb. While there was a tendency to draw the entire hand slightly larger (by about 10 %), this was not statistically significant for the group. Based on group data, the change in perceived size occurred for the anaesthetized thumb but not for the adjacent, unanaesthetized index finger, or other fingers on the same hand (Fig. 2B). In the study with matching templates, there was also no significant change in the perceived size of the index finger adjacent to the anaesthetized thumb. In addition, this study showed that the index finger and thumb on the side contralateral to the anaesthetized thumb did not change their perceived size. However, based on the drawings of an outline of the lips, their perceived size increased during unilateral thumb anaesthesia (by 55 % for the group, P < 0.01). This effect was also significant in eight out of ten subjects. Drawings of the lips before and during anaesthesia were symmetrical with no obvious tendency for the left or right sides to be distorted.
Figure 2. Changes in perceived size of an anaesthetized thumb measured with two methods
A, changes in perceived size of thumbs and index fingers during complete anaesthesia of the left thumb. Anaesthesia was produced by injection of lignocaine around the digital nerves 1 cm distal to the metacarpophalangeal joint. Hands rested palm downwards and vision was excluded. Estimates were made by selection of line-drawing templates which best matched the perceived size of the body part (see Methods). Data from 6 subjects (means ±s.e.m.). Full recovery occurred 2-3 h after the onset of anaesthesia. ▪, left thumb; □, right thumb; •, left index finger; ○, right index finger. B, changes in perceived size of digits on the right hand and of the lips during anaesthesia of the right thumb assessed with the drawing method. Subjects drew around the perceived outline of the body part (see Methods). Means ±s.e.m., 10 subjects. *P < 0.01.
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In complementary experiments, marked (but not complete) anaesthesia of the lips using topical anaesthetics significantly increased their perceived area. This increase occurred when tested with template matching (by an overall mean of 31 %, P < 0.01; also significant in 7 of 11 subjects) or with line drawing (by 60 %, P < 0.01; 9 of 11 subjects). Perceived area of both left and right thumbs increased slightly (by 5 %, P < 0.05) using the template method. This increase was present for six subjects for the left thumb and seven for the right one. With the drawing method the small increases in perceived size of the thumbs (by 4-5 %) were not significant for the group.
Given that removal of the usual sensory input from the thumb caused perceived enlargement of the thumb, we assessed whether an increased sensory input altered perceived size. The changes produced by stimulation of the thumb were smaller than those evoked by anaesthesia. In one study, digital nerves of the thumb were stimulated at an innocuous intensity which produced painless paraesthesiae referred to the tip of the thumb. This was designed to increase the input in large-diameter cutaneous (and joint) afferents. Perceived size of the stimulated digit increased (by 15 % for thumb, P < 0.01, Fig. 4A). This was evident in ten subjects, with one showing a decrease. Perceived size of the lips also increased (by 11 %; P < 0.05, evident in 8 of 11 subjects, Fig. 4A). In a separate study, stimulation of the index finger increased its perceived size (by 25 %, P < 0.01), without a consistent change in size of the adjacent thumb or middle finger.
Figure 4. Changes in perceived size of the digits when the input from them is increased
A, changes in perceived size of thumb and lips during artificial stimulation of the thumb (means ±s.e.m., 11 subjects). Stimuli were delivered through soft electrodes at about 1.5 times sensory threshold for single stimuli at 75 Hz for 1-2 s. Data were obtained with the template-matching method. B, changes in perceived size of the right thumb and lips during cooling of this thumb to a painful degree (means ±s.e.m., 11 subjects). Data were obtained with the template matching method. *P < 0.05.
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To study the effect of an increase in input from small-diameter afferents the distal phalanx of the right thumb was cooled to painful levels by repeated immersion in a water/ice mixture for 1-2 min. The cooled thumb grew in perceived size (by an overall mean of 10 %; P < 0.05; evident in 8 of 11 subjects, Fig. 4B). There was a small but significant reduction in the perceived size of the contralateral thumb (by 4.7 %, P < 0.02). In addition, the lips increased in size during thumb cooling (by 5 % for the group, P < 0.02). For the lips, perceived size increased significantly in six subjects, decreased in one and there was no change in the remaining subjects. The apparent size of the right index finger did not change.
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The main physiological observation in this study is that the perceived size of parts of the body can change rapidly when the afferent input from the part is altered. During anaesthesia of the thumb or lips subjects do not report them as ‘missing’ from the body, an effect which might occur had they simply monitored the amount and spatial distribution of peripheral input. Instead, subjects note a dramatic increase in perceived size when the part is anaesthetized. The results do more than confirm neurological opinion that a body schema remains when the sensory input is prevented from reaching the cerebral cortex following deafferentation, amputation or spinal cord transection (e.g. Head & Holmes, 1912; Melzack & Bromage, 1973).
The changes in perceived size were documented for anaesthesia of the thumb and lips using two psychophysical techniques. One involved matching apparent size to one of a set of templates and the other required drawing of the parts. The apparent enlargement of the thumb during anaesthesia of its digital nerves was of a similar magnitude when assessed by the two methods. The increase in (two-dimensional) area of the thumb would represent a doubling of its volume. Because subjects drew the anaesthetized thumb as larger, the perceptual distortion introduced by anaesthesia is able to disrupt motor performance. Smaller increases in perceived size were documented when the afferent input from the digit was increased, either by activation of its large-diameter afferents with non-painful electrical stimulation, or by activation of small-diameter afferents with painful cooling.
Although these types of perceptual change have not, to our knowledge, been measured previously, they are not necessarily surprising: many subjects reminded us that the lips, tongue and other parts of the face feel enlarged following dental anaesthesia. Furthermore, a well-known phenomenon, often depicted by cartoonists, is the growth in ‘size’ of the thumb when struck a painful blow by a hammer. The perceived increase is more dramatic than any actual increase produced by the blow.
A possible explanation for our findings is that the increases in perceived size with anaesthesia of the thumb (or the lips) are related to the unmasking of inputs to relevant primary somatosensory cortical cells after deafferentation. Acute removal of the afferent input from one digit (by anaesthesia) enlarges the size of receptive fields of cortical cells which represent skin areas adjacent to the site from which the input was removed (e.g. Calford & Tweedale, 1988, 1991a). This is likely to be associated with an increase in the background discharge not only of the cells which can normally respond to input from the anaesthetized part (and particularly its edges), but from a population of cells which receives a subliminal input from a wider area than just the anaesthetized part (Rasmusson et al. 1992). Perhaps these changes in a particular representation are interpreted as consistent with an increased size of the body part. One implication of this possibility is that illusory increases in size may not occur when a large part of the body is anaesthetized or removed because regions of somatosensory cortex devoted to the removed part become ‘silent’ (e.g. Merzenich et al. 1983; Li et al. 1994). This fits with the observation that, when the whole arm is anaesthetized, it is perceived as foreshortened and closer to the body (Melzack & Bromage, 1973). While short-term enlargements in the receptive fields of cortical neurones after deafferentation of a digit may contribute to the changes in perceived size, additional factors are likely to operate. Some receptive fields enlarge in the contralateral homologous cortex after acute deafferentation (Calford & Tweedale, 1990), but perceptual changes were not observed on the contralateral side during thumb anaesthesia.
Why did enhanced input in large- or small-diameter afferents increase the perceived size of the thumb, although to a smaller extent than anaesthesia? The input producing the changes in perceived size was substantial (either repetitive stimulation of the digital nerves or painful cooling of the whole thumb) and would rarely if ever have been encountered prior to these experiments. Interestingly, peripheral nerve stimulation can increase the size of receptive fields of neurones in the primary somatosensory cortex of the cat (Recanzone et al. 1990). Thus, intense or synchronous inputs may produce convergence onto cells and alter their behaviour in ways qualitatively similar, at least in terms of receptive field size, to that following focal deafferentation. Alternatively, or in addition, there may be an important contribution of subcortical interactions to the effects observed with peripheral stimulation.
An increased input in a class of C fibres which were cold sensitive and produced a sensation of pain also distorted the body image. The painful thumb felt larger than under control conditions. This result has implications for distortions of perception associated with small- and large-fibre inputs in states of acute and chronic pain. Some C fibre inputs act tonically to limit the receptive fields of primary somatosensory cortical neurones (Calford & Tweedale, 1991b) such that their removal with capsaicin expands receptive field size. However, other interactions between small- and large-fibre inputs from somatotopically related parts occur at subcortical sites, including the dorsal column nuclei (e.g. Pettit & Schwark, 1996; Dykes & Craig, 1998) and dorsal horn (e.g. Cook et al. 1987).
This study does not reveal the site or sites for the neural interactions leading to the changes in perceived size of the lips when the input from the thumb is altered. However, it could involve cortical and subcortical sites at which the inputs from the thumb and lips are anatomically close. Inputs from the thumb and lips are adjacent within the primary and secondary somatosensory areas of primates (e.g. Robinson & Burton, 1980; Cusick et al. 1989, their Fig. 3; Lin et al. 1994) and also in the thalamus (Jones & Friedman, 1982; cf. Loe et al. 1977). Indeed, based on extracellular recordings in the monkey, some cells in the second somatosensory area have convergent inputs from both thumb and lips (Robinson & Burton, 1980). Furthermore, some cells in the primary somatosensory area of the anaesthetized monkey respond to inputs from the thumb and the lips or chin (Calford, 1997). Input from the lips projects bilaterally to somatosensory areas (Lin et al. 1994) and this may explain why the perceptual distortions showed no obvious left-right asymmetry when the input from the lips (or thumb) altered. A limitation with many estimates of somatosensory ‘maps’ is that they are rarely based on intracellular recordings which are needed to define the full range of subthreshold peripheral inputs to a cell (e.g. Smits et al. 1991). In addition, peripheral and other inputs to the somatosensory cortex may act to restrict receptive field sizes (e.g. Calford & Tweedale, 1991b;Rasmusson et al. 1992).
Figure 3. Line drawings of the thumb and lips before and after anaesthesia of the thumb
Drawings from one subject of the outline of the lips and the right hand before (left) and after (right) anaesthesia of the right thumb. Three typical traces are superimposed. The size of both the anaesthetized thumb and the (unanaesthetized) lips have increased after local anaesthesia.
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Changes in the thumb input failed to alter significantly the perceived size of the adjacent index finger. One possibility is that the boundaries between the thumb and lip representations are functionally less ‘distinct’ than those between the thumb and index finger. There is some indirect evidence for this. Studies of syndactyly suggest that functionally independent digits have more localized cortical representations (e.g. Allard et al. 1991). Somatosensory area 3b for the human thumb is further from the index area, while non-thumb digits are represented closer together (Mogliner et al. 1993, their Fig. 1E). Because human manipulative skill depends so much on the simultaneous differential control of the index finger and thumb, both evolution and development may have required particularly distinct cortical representations for these digits. Furthermore, some kinaesthetic skills are more highly developed for the thumb than other digits (Kilbreath & Gandevia, 1993).
The present results highlight the lability of perceived sizes of body parts and indicate the need to include the sizes of body segments in analysis of kinaesthesia (Gandevia, 1996). Irrespective of the underlying mechanisms, our results provide new ways to expose the sensorimotor consequences of altered peripheral sensory inputs.