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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
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.
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
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
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.
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.
REFERENCES
Aglioti S, Cortese F, Franchini C. Rapid sensory remapping in the adult human brain
as inferred from phantom breast perception. NeuroReport 1994b; 5: 473-476.
Buonomano DV, Merzenich MM. Cortical plasticity: from synapses to maps. Annual
Review of Neuroscience 1998; 21:149-186.
Doetsch GS. Progressive changes in cutaneous trigger zones for sensation referred
to a phantom hand: a case report and review with implications for cortical
reorganization. Somatosensory Motor Research 1997; 14(1):6-16.
Ergenzinger ER, Glasier MM, Hahm JO, Pons TP. Cortically-induced thalamic plasticity
in the primate somatosensory system. Nature Neuroscience 1998; 1 (3): 226-229
Eysel UT Perilesional cortical dysfunction and reorganization. In: Freund HJ, Sabel
BA, Witte OW editors. Brain Plasticity, Advances in Neurology, 73. Lippincott-Raven
Publishers, 1997: 195-206.
Florence SL, Jain N, Kaas JH. Plasticity of Somatosensory cortex in primate. Seminars
in the Neuroscience 1997; 9, 1/2: 3-12.
Halligan PW, Marshall JC, Wade DT, Davey J, Morrison D. Thumb in cheek? Sensory
reorganization and perceptual plasticity after limb amputation. NeuroReport 1993;
4: 233-236.
Halligan PW, Marshall JC, Wade DT. Sensory disorganization and perceptual plasticity
after limb amputation: A follow-up study. NeuroReport 1994; 5: 1341-1345.
Katz J and Melzack R. Referred sensations in chronic pain patients. Pain 1987; 28(1):
51-59.
Kew JJM., Ridding MC, Rothwell JC, Leigh PN, Passingham RE, Sooriakumaran S et al.
Reorganization of cortical blood flow and transcranial magnetic stimulation maps in
human subjects after upper limb amputation. Journal of Neurophysiology 1994; 72:
2517-2524.
Kew JJM, Halligan PW, Marshall JC, Passingham RE, Rothwell JC, Ridding MC et al.
Abnormal access of axial vibrotactile input to deafferented somatosensory cortex in
human upper limb amputees. Journal of Neurophysiology 1997; 77(5):2753-2764.
Luhmann HJ, Mudrick-Donnon LA, Mittman T, Heinemann U. Ischemia-induced longterm hyperexcitability in rat neocortx. European Journal of Neuroscience 1995; 7:
180-191.
Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of
rehabilitative training on motor recovery after ischemic infarct. Science1996b; 272:
1791-1794.
Penfield W. and Rasmussen T. The cerebral cortex of man. New York: Mc Millan
Press, 1950.
Pons T, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. Massive cortical
reorganization after sensory deafferentation in adult macaques. Science 1991;
252:1857-1860.
Recanzone GH, Merzenich MM, Jenkins WM, Grajsky KA, Dinse HR. Topographic
reorganization of the hand representation in cortical area 3a of Owl monkeys trained
in a frequency discrimination task. Journal of Neurophysiology 1992; 67: 1031-1056.
Schroeder CE, Seto S, Arezzo JC, Garragthy PE. Electrophysiological evidence for
overlapping dominant and latent inputs to somatosensory cortex in squirrel
monkeys. Journal of Neurophysiology 1995; 74: 722-732.
Seitz RJ, Freund HJ. Plasticity of the human motor cortex. In: Freund HJ, Sabel BA,
Witte OW editors. Brain Plasticity, Advances in Neurology 73. Lippincott-Raven
Publishers, 1997: 321-333.
Witte OW, Stoll G. Delayed and remote effects of focal cortical infarctions:
secondary damage and reactive plasticity. In : In: Freund HJ, Sabel BA, Witte OW
editors. Brain Plasticity, Advances in Neurology 73. Lippincott-Raven Publishers,
1997: 207-227.
Woolsey CN, Erickson TC, Gilson W. Localization in somatic sensory and motor areas
of human cerebral cortex as determined by direct recording of evoked potentials
and electrical stimulation. Journal of Neurosurgery 1979; 51: 476-506.
Xing J, Gerstein GL. Networks with lateral connectivity. III Plasticity and
reorganization of somatosensory cortex. Journal of Neurophysiology 1996; 75: 217232.
Yang TT, Gallen CC, Ramachandran VS, Cobb S, Schwartz BJ, Bloom FE. Non invasive
detection of cerebral plasticity in the adult human somatosensory cortex.
Neuroreport 1994; 5: 701-704.
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.