Perceptual correlates of massive cortical reorganization
V.S. Ramachandran, D. Rogers-Ramachandran, M. I. Stewart
Science, 1992 Nov 13, 258(5085):1159-60.
Pons et al. (1) found cortical maps to be capable of an
unexpectedly large degree of reorganization. After long-term (12 years)
deafferentation of one limb in adult primates, the cortical area of the
brain corresponding to the limb became responsive to stimuli applied to the
lower face region. This finding extended the previously recognized maximum
area of cortical reorganization in adult primates from a mediolateral
distance of 1 to 2 mm to about 10 to 14 mm. Because cells that originally
received information from the arm can later receive information from the
face, we wondered whether stimuli applied to the face would be mislocalized
to the arm. To explore this, we have studied (2, 3) localization of touch
sensations in two human patients after amputation of one upper limb, and in
another patient after amputation of one digit.
We applied light touch or deep pressure to different points on the normal
body surface. Stimulation of points even remote from the amputation line
evoked precisely localized referred sensations in the phantom limb. We
could plot "reference fields," small regions of skin surface that evoked
referred sensations in specific parts of the phantom limb (for example, the
digits). Our main experimental findings may be summarized as follows:
(i) Points (reference fields) were not randomly distributed. There were two
clusters, one on the same side of the face as the phantom limb, and one
around the line of amputation. Furthermore, there was precise one-to-one
correspondence between these points and those on the phantom limb. (3).
(ii) Sensations were referred most often to the hand, especially to the
digits with an overrepresentation of the thumb and "pinky." This may
reflect the high cortical magnification of these areas. (iii) The referred
sensations were modality-specific; for example, a drop of warm water
trickling down the face was felt as "warm water trickling down"in the
phantom hand. (iv) Reference fields were somatotopically organized. we
suggest that this is a direct consequence of the remapping observed by
physiologists (1). (v) There was a vivid persistence of short-term "memory"
of complex sensations; when we gripped and released the finger adjacent to
the amputated finger the patient felt the phantom finger being "gripped,"
and this sensation persisted for 7 or 8 seconds in the phantom. (v1)
Reorganization was relatively rapid. In one patient, our study was carried
out 4 weeks after limb amputation rather than 12 years.
That patients "refer" paresthesiae to a "phantom limb is in itself not
new. We have attempted to systematically relate such findings to studies of
animal physiology (1, 4). For example, we suggest that the reason we found
two clusters of reference fields exhibiting topography-one on the face and
the other one near the amputation line-is because the hand area in
Penfield's homunculus (in the somatosensory cortex) is flanked on one side
by the face and on the other side by areas around the line of amputation
(for example the upper arm and shoulder). We would therefore expect sensory
input from both these regions to "invade" the cortical hand area and
provide a basis for referred sensations.
The very existence of phantom limbs might be partially explained by our
hypothesis. If tactile and proprioceptive input from surrounding tissue
"takes over" the brain areas corresponding to the amputated limb,
spontaneous discharges arising from neurons innervating these tissues would
be misinterpreted as arising from the missing limb. This hypothesis is
different from, although not incompatible with, the idea that phantom limbs
result from the persistence of a "neurosignature" in a diffuse neuronal
pool (5). Our observation that the changes can occur as early as 4 weeks
after amputation is especially interesting since it suggests that the
reorganization is a result of the unmasking of "silent" synapses rather
than of anatomical changes such as "sprouting." Perhaps, even in normal
adults, input from the face projects simultaneously to both face and hand
areas in the cortex or thalamus (and input from the hand to both hand and
face areas). The unwanted input to the hand area, however, may be subject
to tonic inhibition (for example, through an inhibitory interneuron) by the
"correct"axon carrying a signal from the hand. When an arm is amputated,
this occult input is unmasked through disinhibition. It remains to be seen
whether this unmasking is permanent or whether the patients eventually
begin to "ignore" the referred sensations.
Whatever the ultimate interpretation may be, however, our findings suggest
that the adult mammalian brain has a latent capacity for much more rapid
functional reorganization over a much greater area than previously thought,
a capacity that could conceivably be exploited for therapeutic
purposes.
References
1. T.P. Pons et al., Science 252, 1857 (1991).
2. V.S. Ramachandran, M. Stewart, D.C. Rogers-Ramachandran,
Neuroreport 3, 583 (1992).
3. _____, Soc. Neurosci. Abstr., in press.
4. M.M. Merzenich et al., J. Comp. Neurol. 224, 591 (1984);
P. Wall, Philos Trans. R. Soc. London Ser. B 278, 361 (1977).
5. R. Melzack, Sci Am. 266, 120 (April 1992).
6. We thank patients V.Q., W.K., and D.W. for their cooperation; M. Botte
and R. Abrams for referring them to us; M. Parsa and O. Gil for assistance;
and the Air Force Office of Scientific Research and the Office of Naval
Research for support.