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ANOMALOUS DOUBLE SENSATIONS AFTER DAMAGE TO THE CORTICAL

SOMATOSENSORY REPRESENTATION OF THE HAND IN HUMANS

Salvatore Aglioti1,2, Alberto Beltramello3, Andrea Peru2, Nicola Smania4, Michele


Tinazzi5

1 Dipartimento di Psicologia, Universit La Sapienza, Roma, Italy


2 Dipartimento di Scienze Neurologiche e della Visione, Sezione di Fisiologia Umana,
Universit di Verona, Verona, Italy
3 Servizio di Neuroradiologia, Ospedale Maggiore, Borgo Trento, Verona, Italy
4 Servizio di Rieducazione Funzionale, Policlinico Borgo Roma, Verona, Italy
5 Dipartimento di Scienze Neurologiche e della Visione, Sezione di Neurologia,
Universit di Verona, Verona, Italy

Address for correspondence and reprint requests:


Salvatore M. Aglioti, Universit di Verona, Dipartimento di Scienze Neurologiche e
della Visione, Sezione di Fisiologia Umana, Strada Le Grazie 8, 37134 Verona, Italy
Voice ++39-45-8098134; Facsimile ++39-45-580881; E-mail:
smagli@borgoroma.univr.it

Running Head: ANOMALOUS SENSATIONS AND NEUROPLASTICITY

ABSTRACT

Hand amputees may report that a tactile stimulus delivered to the stump region or
the face ipsilateral to the amputation induces the sensation of being touched on the
phantom. Given the representational contiguity between hand and face, this
phenomenon has been related to electrophysiologically demonstrated orderly
remappings occurring in deafferented somatosensory areas. Here we report for the
first time double sensations evoked by tactile stimuli delivered to the contralesional
hypoesthesic hand in a patient with a lesion involving the hand representation in
the primary somatosensory cortex. These double sensations were very precise and
consistent over a 4-months period and were clustered on the contralesional scalp
and bilaterally on the nape. The distribution of the referred sensations did not
conform to any orderly topographic relation with the known somatosensory hand
representation. Since in our patient the lesion left unaffected the nervous pathway
from the skin to the thalamus, the selective cortical perturbation may have induced
a thalamic reactivity eventually leading to the expression of latent thalamic inputs
to intact cortical targets. The non-topographic distribution of the areas inducing
double sensations is likely to reflect a noisy rearrangement process.

KEY WORDS: SOMATOSENSORY CORTEX - BRAIN DAMAGE - ADULT HUMAN BRAIN NEURAL REARRANGEMENT- BRAIN PLASTICITY - SENSORY
DISORGANIZATIONINTRODUCTION

Psychophysical testing in amputees who experience phantom perceptions has


shown that specific sensations referred to the amputated body parts can be evoked
by tactile stimuli delivered to select cutaneous regions (Cronholm, 1951). In some
cases the skin areas from which veridical and referred sensations can be evoked are
represented in the brain in an orderly relation with the representation of the
amputated part. For example, following amputation of a hand, stimulation of the
lower hemiface or neck ipsilateral to the amputation may elicit, in addition to the
local sensation, the feeling of being touched on the phantom fingers or index or
palm (Ramachandran et al., 1992; Halligan et al 1993; Aglioti et al., 1997; Doetsch,
1997). It is known that the face and the hand are represented close to each other in
the somatosensory system at both cortical and subcortical levels (Penfield and
Rasmussen, 1950; Woolsey et al., 1978). The anomalous double sensations may
indicate the extent to which sensory inputs from the face and neck have occupied
somatosensory regions formerly representing the amputated hand; thus, this
phenomenon may represent a possible perceptual correlate of the remapping
phenomena observed following peripheral denervation in somatosensory and motor
systems of human and other primates with electrophysiological, brain imaging and
magnetic stimulation techniques (Pons et al., 1991; Yang et al., 1994; Kew et al.;
1994,1997; Boorsook et al., 1998). Recent magnetoencephalography studies,
however, found that indices of reorganization in primary somatosensory areas are
positively correlated with phantom pain but not with non-painful phantom
sensations (Flor et al., 1995; Knecht et al., 1996; 1998). Moreover, the distribution
of skin regions evoking phantom sensations may be quite variable and inconsistent
with a strictly topographic remapping. However, although the phenomenon of
evoked phantom sensations may not be a precise landmark of the amount of neural
remapping, it has to do with changes in the adult nervous system induced by
perturbations of the peripheral inputs.
So far, psychophysical studies of anomalous sensations possibly related to
reorganizational changes in the adult brain have been mainly carried out in
amputee patients who do not have any damage to the central nervous system. The
extremely important issue of reorganizational changes after brain lesions has been
addressed recently in both animal (Nudo et al., 1996a, 1996b; Xerri et al., 1998) and
human studies (Chollet and Weiller, 1994; Seitz and Freund, 1997). It may be
relevant for rehabilitation to try and see if the simple psychophysical approach used
in amputees may be helpful in revealing anomalous evoked sensations also in
patients with lesions of the central nervous system. A potentially interesting model
for testing this hypothesis in humans is the assessment of brain damaged patients
with small cortical lesions involving selectively parts of a given representation, for
example the hand. Since in these patients the nervous pathway from the skin to the
thalamus is intact, one may wonder whether thalamic fibers disconnected from the
lesioned cortex are able to express their relation with other cortical targets. This

hypothesis is supported by the notion that cortical neurons may receive dominant
and latent inputs from different body parts (Schroeder et al., 1995; Xing and
Gerstein, 1996). Were this the case, should it be possible that somatic stimuli
delivered to the hypoesthesic (or even the anaesthesic) skin regions (e.g., the hand)
are mislocated to skin regions mapped contiguously in the cortex (e.g., the face
ipsilateral to the lesion) just like in amputee patients? Indeed, in these braindamaged patients not only the nervous pathway from the skin to the thalamus is
intact, but also specific parts of the thalamo-cortical sensory pathway may be
unaffected by the lesion. A major problem with this model is related to the
possibility of finding in humans select and quite small cortical somatosensory
lesions. Nevertheless, we report here the presence of anomalous double
sensations evoked by somatic stimuli in a patient with a small lesion involving the
S1 hand representation.

MATERIALS AND METHODS


Subjects. We tested two right-handed women (CG and GT) with an ischemic lesion
mainly involving the somatosensory cortices and one right-handed man (GV) with
an haemorrhagic lesion centred upon the posterior part of the right thalamus.
Manual preference was assessed in all patients by using the Briggs and Nebes'
(1975) laterality inventory. The patients were selected because they presented with
clear somatosensory deficits but their elementary motor functions (e.g., muscle
strength and tone) were practically unimpaired.
Patient CG: is a 51-year old housewife with 5 years of schooling. On October 3, 1995
she suddenly suffered from paresthesias to the right hand and a great difficulty in
feeling and holding objects with that hand. No other neurological or
neuropsychological signs were detected. A MRI exam performed on November 27,
1995 documented a small ischemic lesion involving the left primary somatosensory
cortex (Figures 1 and 2).
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PLEASE INSERT FIGURES 1 AND 2 NEAR HERE
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When we first met this patient, 18 days after the stroke, she exhibited a severe
somatosensory deficit in the right hand with which she was unable not only to
recognise but also, in several trials, to detect the presence of common objects put
there by the examiner. We found only minimal sensory deficits in the right forearm
and no deficit at all in the right arm and shoulder. Deep tendon reflexes were
normal. Active movements of the hand appeared normal under visual guidance, but
were awkward and imprecise when the patient was blindfolded. The sensory deficit,
confined to the right hand and wrist, was clearly expressed in the patient's inability
to localise tactile stimuli delivered to those regions. Pinpricks delivered to the right
fingers were perceived but not localised correctly. Unlike the other two patients, CG
was able to detect the movement of tactile stimuli sliding on her right hand, but was

inaccurate in reporting the direction of the movement. Position sense was impaired
at the fingers and wrist but it was comparable to the other side at the elbow and
shoulder. Vibratory stimuli to the right fingers were perceived but not localised. The
perceived duration of vibratory stimuli was longer on the intact side by 8.5 sec at
the thumb, 8 sec at the index finger, 8 sec at the middle finger, 7 sec at the ring
finger, and 8 sec at the little finger. Smaller left-right differences of 4 and 2 sec
were recorded at the wrist and the elbow, while no side differences for vibratory
stimuli were observed at the cheekbone.
Patient GT was 68 year-old at the time of the present study. She had suffered
(when she was 59) from a lesion centred upon the right primary somatosensory
area but involving in part the posterior parietal cortex and a small part of the right
temporal superior gyrus. Detailed information on this patient is reported elsewhere
(Aglioti et al., 1996). A clinical examination showed somatosensory deficits
particularly severe at hand and wrist. No tactile stimulus delivered to the hand was
localised correctly and only intense pinpricks were detected.
Patient GV is a 51-year-old street-cleaner with 5 years of schooling who
suddenly suffered from motor weakness and loss of sensibility to the right
hemisoma. A MRI examination showed a hyperdense, haemorrhagic lesion involving
the left thalamus and the overlying white matter. When we met the patient, 12 days
after the stroke, there was no residual motor impairment. By contrast, he showed a
clear hemianesthesia which was particularly severe at the right hand where only
vibratory stimuli and very intense pinpricks could be detected. The perceived
duration of vibratory stimuli was longer on the intact side. The right-left difference
was 9.5 sec. at the basis of the index finger, 8.5 at the wrist and 7 at the elbow. A
marked difference (6.5 sec) emerged also for stimuli to the cheekbone. No stimuli to
the upper right limb were localised correctly. All patients badly failed a hatpic test of
object recognition by scoring 0 hits out of 20 trials. None of them was able to judge
whether objects held in the two hands were the same or different. During standard
procedures for examining tactile functions, we serendipitously noticed that patient
CG was puzzled by the occurrence of anomalous double sensations when touched
on the hypoesthesic skin regions. With the aim of investigating this phenomenon
systematically, we tested all the three patients as follows: In a preliminary
interview, they were questioned about any anomalous sensations that may had
occurred after their stroke (how long they had lasted, when they had started and
whether or not they were still present at the testing period). During the testing
sessions, patients were required to report on the sensations elicited by somatic
stimuli delivered to several skin points both ipsilateral and contralateral to the
lesion. In the first testing session at least five stimuli were delivered to each of the
following points: dorsal and ventral surfaces of foot, leg, thigh, forearm, arm,
shoulder; anterior and posterior surface of the neck, four points on the face, dorsal
and ventral surfaces of the hand, fingers and wrist. Stimuli could be delivered both
within and outside the hypo/anaesthetic areas. Different kinds of somatic stimuli
were used: light touch and sliding stimuli were delivered by using the examiners
fingertips, deep pressure through the handle of a knee hammer, pinpricks through
the tip of an esthesiometer. Patients were instructed to keep their eyes closed

during stimulations. Accuracy of response was recommended. The possible


presence of a response bias was checked by introducing catch-trials, i.e. trials
where no stimulus was delivered after the examiners warning. Patient CG
spontaneously reported anomalous double sensations contingent upon stimulation
of the hypoesthesic hand. Patients GT and GV, who never reported evoked double
sensations, were explicitly encouraged to pay attention about any possible double
sensation evoked by stimuli delivered by the experimenter. All patients consented
to participate in the testing. While all patients were informed that the test was not
part of any rehabilitation programme, none of them was informed about the aims of
the experiment. A different number of trials were delivered in the different
experimental sessions. This was mainly due to the patients fatigue and other
controls or exams scheduled for the session. The interval between stroke and first
testing session was 73 and 40 days in patients CG and GV and about 8 years in
patient GT.

RESULTS
In no trials did patients commit false alarm errors, as they never reported nondelivered stimuli. In two sessions separated by a two-week interval, GT and GV
never reported any stimulus-induced double sensations or sensations mislocalized
to body points different from that stimulated. By contrast, CG reported that single
stimuli delivered to her affected hand evoked a sensation remote from the
stimulated point in addition to a veridically localised sensation. Since CG is the only
patient who showed this phenomenon we focus hereafter on her performance. The
presence of anomalous double sensations in patient CG was tested systematically
in 4 sessions (73 days, 106 days, 146 days and 9 months after the stroke). Double
sensations were evoked only by stimuli on the hypoesthesic regions. The remote
skin regions where the anomalous double sensation was referred to were clustered
on the scalp contralesional to the hypoesthesic hand and on the posterior part of
the neck, bilaterally. The distribution of these regions was consistent over the first
three sessions. A schematic drawing of areas of mislocalization of stimuli delivered
to the hypoesthesic regions is reported in figure 3. The testing sessions were
videotaped and reconstruction of referral areas was checked against the film
sequences.
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PLEASE INSERT FIGURE 3 NEAR HERE
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Quantitative results are reported in table 1.
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PLEASE INSERT TABLE 1 NEAR HERE
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Although the localisation was not as precise as in some amputee patients, the
patient reported to be sure that the anomalous double sensation was identical to
the sensation originating from the hypoesthesic region. For example, sliding stimuli
were reported as slides on the scalp or nape, displacement of a finger evoked a
sensation of movement also on the scalp. The patient stated the following: I know,
you can hardly believe me; however, what I feel on the scalp is what I feel when you
touch my hand. This pattern of response was also consistent over 3 testing
sessions. According to the patients report strong stimuli evoked clear double
sensations. The simultaneous stimulation of points on the hypoesthesic hand and
scalp or nape did not modify the perceptual quality of the anomalous double
sensations. Two simultaneous stimuli within the hypoesthesic area elicited double
sensations on the scalp that were strong but less well localised. Anomalous double
sensations were identical when evoked by a single stimulus on the hypoesthesic
hand or by two stimuli delivered to symmetrical points on the two hands. The
patient was able to evoke double sensations by auto-stimulating her affected hand
with a pencil (in 5 out of 5 trials) and with her left index (in 2 out of 5 trials). In no
case did stimuli delivered to the referral areas (scalp or neck) evoke any double
sensations. No anomalous double sensation was evoked in the testing session
carried out 9 months after the stroke when somatosensory deficits had only partially
cleared-up. A schematic representation of somatosensory deficit and presence of
referred sensations over the different sessions is reported in table 2.
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PLEASE INSERT TABLE 2 NEAR HERE
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DISCUSSION
Recent studies have shown a considerable reorganizational power in the adult
brain as a consequence of learning (Recanzone et al., 1992; Merzenich and
Sameshita, 1993) or deafferentation (Florence et al., 1997; Buonomano and
Merzenich 1998). Even more novel is the notion of considerable neural
rearrangements following lesions to the central nervous system in non-human
(Nudo et al., 1996a, 1996b; Xerri et al., 1998) and human primates (Chollet and
Weiller, 1994; Seitz and Freund, 1997).
The present report shows for the first time that anomalous double sensations can be
evoked systematically in a patient with a lesion of the primary somatosensory
cortex. The phenomenon shows some limited analogies with the phantom
sensations evoked by tactile stimulation of intact skin regions in limb or breast
amputees (Cronholm, 1951; Aglioti et al.; 1994a; 1994b; 1997; Ramachandran et
al., 1992; Halligan et al., 1994; Knecht et al., 1996; 1998). Anomalous double
sensations evoked by electrical stimulation of the pinna have been reported in
chronic low-back pain patients (Katz and Melzack, 1987). It is noteworthy that a
recent magnetoencephalography study in low-back pain patients has shown clear

signs of reorganization in the primary somatosensory cortex (Flor et al., 1997).


Findings from our patient also present some analogies with data from neurologically
intact subjects submitted to a prolonged vibratory stimulation of the volar surface of
the forearm. After a 5-9 week period of repetitive stimulation, these subjects
mislocalised tactile stimuli delivered within the previously vibrated skin area;
moreover, they reported as double or triple, single stimuli delivered to the vibrated
regions (Craig, 1993). These anomalous sensations disappeared within 15 weeks
from the interruption of the repetitive stimulation. It appears that only the absentminded wearing of vibrators can induce double sensations; indeed, people who
wear vibrators as aid for blindness, and then attend the vibration stimuli, do not
report any anomalous sensations (Craig, 1993). These results are in keeping with
the notion that only plasticity effects linked to learning tasks are highly specific and
probably require attention (Recanzone et al., 1992). Thus, stimuli not relevant for
behaviour are not attended to and may simply introduce unwanted noise in the
functioning of the system.
Although it is hard to tell why anomalous double
sensations are detected only in patient CG, some variables possibly involved in the
phenomenon are to be discussed. The interval between stroke and testing may play
a role because remote functional alterations after stroke may be maximal soon after
the insult. However, this variable is unlikely to play a crucial role because both CG
and GV have been tested in the acute post-stroke phase but only the former
presented with referred double sensations. The severity of the somatosensory
deficit and the type of lesion may be relevant variables. Patient CG not only
presented with the mildest somatosensory defect but she also had the smallest
cortical lesion and a complete sparing of the thalamus. These two conditions may
leave room for reorganizational changes that may be linked to hyperactivity in
perilesional areas, isles of spared neurons within the lesion, or the thalamus. The
type of cortically induced thalamic plasticity recently described by Pons and coworkers may play a role in the above-described phenomenon. These authors
(Ergenzinger, Glasier, Hahm and Pons, 1998) used a NMDA receptor antagonist to
inactivate the hand representation into the area 3b and found a dramatic
enlargement of the receptive field of thalamic neurons representing the hand. This
is not to say that the thalamus is the source of double sensations in our patient but
rather that an increased thalamic reactivity may allow the expression of thalamocortical connections kept silent under normal conditions. A long-term
hyperexcitability consequent to an experimental induced ischemia has been
documented in carefully controlled animal studies and put in relation to plastic
processes following brain lesions (Eysel, 1997; Witte and Stoll, 1997). Such an
hyperexcitability may be present not only ispilaterally and nearby the ischemic
lesion, but also in brain areas remote from the lesion (Witte and Stoll, 1997). It is
also noteworthy that this effect, perchance related to a dysregulation of the
gabaergic system, may last from a few weeks to several months (Luhmann,
Mudrick-Donnon, Mittman and Heinemann, 1995; Neumann-Haefelin, Staiger,
Redecker, Zilles, Fritschy, Moheler, et al. 1998). This lapse of time suggests some
analogies with the time of disappearance of evoked double sensations reported in
our patient that may thus be expression of a post-lesional hyperactivity.

In patient CG, the loci of mislocalized sensations turned out to be quite consistent
over the experimental sessions but did not seem to bear any orderly topographic
relation to the central representation of the hypoesthesic hand. In amputee
patients, or at least in some of them, phantom sensations are evoked by stimulation
of skin regions whose central representations border on those of the amputated
body part. Doetsch (1997) reported a hand amputee patient in whom skin areas
evoking phantom sensations changed size and site but remained topographically
referred to specific fingers and other parts of the phantom hand, both soon and one
year after the amputation. Other follow-up studies of limb amputees (Halligan et al.,
1994; Aglioti et al., 1997) suggested that a topographic pattern of functional
somatosensory rearrangement may be limited to an initial period following
amputation and is related to sensations that are relevant for behavioural control.
Thus, the fact that evoked double sensations in patient CG were no longer present
nine months after the stroke also hints at a variability of reorganization processes
with an eventual disappearance of sensations that are not used during daily life
behaviour. This in keeping with the report in normal human observers that
scratching a small excrescence on the skin may be referred to distant points as a
prick or a tingle (Richter, 1977). Interestingly, this referral phenomenon appears to
occur only during absent-minded scratching of the skin, i.e. when attention is not
focused on the local sensation produced by the scratch. A more complex pattern of
reorganization in amputees has been suggested by Knecht et al. (1998) who found
that while the amount of cortical reorganization inferred from
magnetoencephalography recording is rather stable, the topography of evoked
sensations changes considerably over time perhaps because the alterations of
sensory processing are mediated by extensive networks with fluctuating synaptic
strengths.
In conclusion, the application of the simple psychophysical paradigm used in
amputees (Raamchandran et al., 1992; Aglioti et al., 1994a;1994b;1997) allowed us
to find a perceptual phenomenon that may have to do with neural rearrangement
processes consequent to a very small lesion affecting selectively the area of
representation of the right hand. However, the finding does not imply that this type
of anomalous evoked sensations have any functional relevance; it is noteworthy
that no representational contiguity between hypoesthesic areas and areas of
reference of stimuli has been reported. Thus, the phenomenon cannot be explained
in terms of topographic rearrangement; however it speaks to the case that erratic
changes in neural connectivity ensue from lesions of the central nervous system.

ACKNOWLEDGEMENTS Thanks are due to Prof. G. Berlucchi for his valuable


comments and to Mr. Marco Veronese for preparing the figures. The financial
support from the M.U.R.S.T. and the Consiglio Nazionale delle Ricerche, Italy to S. M.
A. is gratefully acknowledged.

FIGURES AND TABLE CAPTIONS

Figure 1: Select MRI cuts (T2-weigthed coronal) in patient CG. Only slices in which
the lesion was detected are reported. The upper left and the lower right pictures are
the most anterior and the most posterior cuts respectively. It appears that the lesion
(marked by arrows) is confined within a select portion of the post-central gyrus.

Figure 2: Select MRI cuts (T2-weigthed transverse) in patient CG. Only slices in
which the lesion was detected are reported. The upper left and the lower right
pictures are the most caudal and the most rostral cuts respectively. The lesion is
marked by arrows.

Figure 3: Somatic stimuli applied to the hypoesthesic regions were referred to the
regions of skin indicated as A and B. Stimuli were delivered to both palmar and
dorsal surface of the hand and fingers.

Table 1: Number of somatic stimuli delivered to points within the hypoesthesic


region in each experimental session. No stimuli delivered outside the hypoesthesic
skin regions evoked double sensations. Stimuli delivered to the hypoesthesic areas
evoked referred sensations in at least 95 % of trials. In a fourth testing session
carried out 9 months after the stroke no anomalous double sensations could be
evoked by stimuli on the hypoesthesic hand. Legend: Tr.= total number of stimuli;
Ref. Scalp and Ref. Nape indicate the number of trials in which anomalous double
sensations were referred to areas marked as A and B in figure 3. The difference
between numbers under the heading Tr. and Ref. indicates trials in which no double
sensation was evoked.

Table 2: Somatosensory deficit and presence of referred double sensations in the


different testing sessions. Aspects of the deficit relevant for the assessment of
double sensations are plotted. Legend: Refer. Sens.: referred double sensations, see
also table 1 and figure 3. Stim. Det: detection of stimuli of 20 g; Stim. Loc: capability
to localize the above stimuli; Stim. Dir: capability to judge the direction of sliding
stimuli; Texture recog.: the patient was required to judge as same or different two
different textures; Hap. Objec. Rec: capability to recognise objects held in the
affected hand. It is noteworthy that in the first session only, the patient resulted
unable to even feel the presence of the object in 4 out of 20 trials. Values represent
the percentage of correct detections (out of 16 trials, except than in the haptic
object recognition test) of stimuli delivered on the affected hand and wrist.

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Title: Anomalous double sensations after damage to the cortical somatosensory


representation of the hand in humans

Authors: S Aglioti, A Beltramello , A Peru, N Smania, M Tinazzi

Abstract: Hand amputees may report that a tactile stimulus delivered to the stump
region or the face ipsilateral to the amputation induces the sensation of being
touched on the phantom. Given the representational contiguity between hand and
face, this phenomenon has been related to electrophysiologically demonstrated
orderly remappings occurring in deafferented somatosensory areas. Here we report
for the first time double sensations evoked by tactile stimuli delivered to the
contralesional hypoesthesic hand in a patient with a lesion involving the hand
representation in the primary somatosensory cortex. These double sensations were
very precise and consistent over a 4-months period and were clustered on the
contralesional scalp and bilaterally on the nape. The distribution of the referred
sensations did not conform to any orderly topographic relation with the known
somatosensory hand representation. Since in our patient the lesion left unaffected
the nervous pathway from the skin to the thalamus, the selective cortical
perturbation may have induced a thalamic reactivity eventually leading to the
expression of latent thalamic inputs to intact cortical targets. The non-topographic
distribution of the areas inducing double sensations is likely to reflect a noisy
rearrangement process.

Journal: Neurocase
Neurocase Reference Number: 239/98
Primary Diagnosis of Interest: Somatosensory deficits
Authors designation of the case: CG
Key Theoretical issue: Post-lesional plasticity
Key words: somatosensory cortex - brain damage - adult human brain - neural
rearrangement- brain plasticity - sensory disorganization
Scan, EEG and related measures MRI scan
Standardized assessment: Clinical examination of somatosensory functions
Other assessment: Assessment for double sensations
Lesion location: left somatosensory cortex
Lesion type: ischemic stroke
Language: English

Aglioti et al.

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