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Annu. Rev. NeuroscL1991.14:137~57
Copyright©1991by AnnualReviewsInc. All rights reserved
PLASTICITY OF SENSORY
AND MOTOR MAPS IN
ADULT MAMMALS
Jon H. Kaas
Department of Psychology, Vanderbilt University, Nashville,
Tennessee 37240
KEY WORDS:
spinal cord, thalamus,
nerve regeneration
auditory
system, ventroposterior
nucleus,
INTRODUCTION
This review addresses questions about the capacity of sensory and motor
maps in the brains of adult mammalsto change as a result of alterations
in the effectiveness of inputs, the availability of effeetors, and direct
damage. The issue of the mutability of mapsin adults is important because
sensory and motor representations occupy muchof the brains of mammals,
regardless of the complexity and extent of neocortex (e.g. Kaas 1988,
Wall 1988, Maunsell & Newsome1987); behavioral recovery occurs after
damage to central representations (e.g. Bornschlegl & Asanuma1987,
Diirsteler et al 1987, Eidelberg &Stein 1974); and such changes mayrelate
to improvementsin sensory and motor skills with experience (e.g. Gibson
1953). In addition, features of reorganization that are apparent in sensory
and motor mapsmaycharacterize less easily studied areas of the brain.
Specific questions addressed in this review are as follows:
1. An obvious question is, "Does map reorganization occur in adult as
well as developing mammals?"The mutability of developing sensory
maps as a result of environmental manipulations, especially sensory
deprivation, is well documented and accepted (see Sherman & Spear
1982, Kaas et al 1983, McKinley et al 1987, Wall 1988), but many
changes appear to occur only within a "critical period" of development.
The often less dramatic evidence for alterations in adults may seem
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questionable, open to alternative explanations, or so limited in extent
to be unimportant(see Killackey 1989 for review). Thus, it is useful
consider the nowextensive evidence for mapreorganization in adult
mammals.
Since sensory systems consist of a numberof separate representations
that are interconnected in a semihierarchical fashion, another obvious
and long-standing question is, "What stages are capable of reorganization?" Early evidence for plasticity was obtained at the level of
sensory inputs to the spinal cord (e.g. Liu & Chambers1958, Devor
Wall 1978), and at least some of the changes described in primary
somatosensorycortex could simply result from the relay of subcortical
alterations. There nowis evidence, however, for the restructuring of
mapsat three levels of cortical processing in the somatosensorycortex,
and for changes that cannot be easily attributed to the relay of subcortical reorganizations.
To date, the bulk of the evidence for plasticity in maps stems from
experiments in the somatosensory system. Thus, "Are other sensory
and motor systems capable of reorganization?" Recent experiments on
the motor, visual and auditory systems suggest that the capacity to
rcorganizc characterizes all central representations and maybe a general
feature of brain tissue.
"How rapidly does cortex reorganize?" This is an important issue
because different mechanisms have been proposed for rapid and slow
alterations.
"What are the magnitudes of the observed changes?" Small alterations
are compatible with synaptic and other modifications within previously
existing structural frameworks, whereas larger modifications mayimply
the sprouting and growth of new connections.
Finally, "Whatare the relative extents of changes at different stages
of sensory hierarchies?" These are critical to evaluate because higher
stations have been hypothesized to be more plastic (e.g. Merzenichet
al 1988, Pons et al 1988).
Muchof the research on the plasticity of neural mapsin adult mammals
has been on primary somatosensory cortex. Primary somatosensory cortex
is a convenient place to look for plasticity in the somatosensory system
because S-I contains a relatively large, two-dimensional mapthat in many
species is largely accessible on the dorsolateral surface of the brain.
Changesin the smaller, three-dimensional representations in the brainstem
and spinal cord are more difficult to demonstrate, and the higher order
maps in cortex can be less responsive to sensory stimuli under typical
recording conditions and can have more complex maps in which changes
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PLASTICITY
OF SENSORY
AND MOTOR MAPS
139
in the representation maybe less obvious. Thus, it has been logical and
productive to look for plasticity in S-I.
REORGANIZATION
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(AREA 3B)
OF S-I
OF MONKEYS
A number of experimental approaches have demonstrated somatotopic
changes in the representation of skin receptors in area 3b or $-I proper of
monkeys. Although the term S-I has been used to include up to four
separate representations in monkeysand higher primates, only area 3b
appears to be the homologof primary somatosensory cortex or S-I of the
nonprimates (Kaas 1983). A popular site of investigation has been area
3b of somatosensorycortex in the relatively unfissured brains of such New
World monkeys as owl monkeys, squirrel monkeys, and marmosets. These
and other monkeyshave a large, central portion of area 3b devoted to the
glabrous or ventral surface of the hand (Figure 1A; also see Merzenichet
al 1978, Sur et al 1982, Carlson et al 1986). The arrangementof skin parts
on the ventral hand (Figure 1B), the palmar pads, and glabrous phalanges
is preserved but distorted in the cortical map(Figure 1C). Each digit
represented in order, with proportionally more cortex devoted to the
sensitive digit tips. The spatial arrangementof the palmar pads, allowing
for a partial split of the palm betweenthe thenar and hypothenar pads, is
also maintained. The representation of the dorsal or hairy skin of the hand
occupieslittle tissue, and the location of dorsal skin in the mapis variable
across and within species. The representation of the back of the digits and
hand, however, is often split into separate locations lateral and medial to
the representation of glabrous skin (Figure 1 C) and into islands of cortex
within the representation of glabrous skin.
The Effects of Removin9an Input
Cutting or crushing the median nerve, which subserves the thenar half of
the glabrous hand from D1 through the middle of D3, produces, over
time, a dramatic change in map organization (Merzenich et al 1983a,
Huerta et al 1986). The nerve section, by deactivating inputs from half of
the hand, deprives a large lateral sector of the hand representation in area
3b of its normal source of activation (Figure 1D). Before regeneration
occurs, the deprived cortex becomesresponsive to new inputs largely from
the dorsal surface of the hand but also from parts of the palmar pads with
preserved cutaneous innervation. There is no recovery of responsiveness
to the denervated skin, apparently because intact nerves have a very limited
capacity to sprout and claim vacant territory (Jackson & Diamond1981,
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140
r~AAS
Kinnman& Aldskogius 1986). A new somatotopic organization is created
in area 3b, the representations of the dorsal surfaces of digits 1-3 become
many times larger than in normal animals, and receptive fields on the
dorsal hand for neurons in this altered cortex are much smaller than
normally seen for cortical neurons representing the dorsal hand. The time
course of the change is not well-known,but someof the reactivation occurs
within hours of the nerve section, and further alterations in responsiveness
and representational detail appear to occur over days to possibly months
(Merzenich et al 1983b).
The effects of deactivating a peripheral nerve can be partly or totally
reversed by nerve regeneration. Regeneration after nerve crush in humans
is typically followed by complete sensory recovery and no notable impairments (see Wall &Kaas 1985 for review). This behavioral recovery apparently reflects complete or nearly complete and errorless regeneration
(Lisney 1983). Recordings from the hand representation in area 3b
monkeysafter nerve crush and regeneration reveal maps that not only
are totally normal (Figure IF), but when the same monkeyis recorded
both before and after nerve crush and regeneration, individual features
of the mapsreturn (Wall et al 1983). These results demonstrate that nerve
regeneration after nerve crush can be extremely accurate, hence the recovery of normal function, and that changes produced during reorganization can be reversed, even to the extent of returning individually unique
features. Althoughthe cortical mapis plastic and it does change after nerve
damage, the recovery of a specific, previous organization indicates that
original connection patterns persist, have some advantage, and previous
activation patterns are likely to reappear.
Another outcome occurs if a nerve is cut, repaired by suturing the cut
ends together, and allowed to regenerate (Paul et al 1972, Wall et al 1986,
1988, 1989b; Figure 1G). After such repair, regeneration is incomplete and
disorderly (Florence et al 1988). The resulting complexof changes in cortex
incorporates (a) sections of reorganized cortex that are not recovered
inputs from the regenerated nerve and (b) sections of somatotopically
disorganized cortex that are activated by the regenerated nerve (Wall et
al 1986). Because nerve regeneration is incomplete, original sources of
activation do not return for some parts of the deprived zone of cortex.
The cortex remains reorganized and responsive to intact inputs from other
nerves. However,disorderly nerve regeneration produces other patches of
cortex that are responsive to median nerve inputs, but these patches do
not form a continuous, orderly, somatotopic map. In addition, neurons in
manyreactivated cortical locations have several, separate receptive fields.
Thus, peripheral axons previously subserving a restricted skin location
regenerate to several different skin locations. Furthermore, somecortical
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PLASTICITY
OF SENSORY AND MOTOR MAPS
141
neurons become abnormally responsive to deep or pacinian receptors,
thereby suggesting that regenerated terminals are established in the median
nerve skin field with inappropriate receptors. The results demonstrate that
there may be no central correction for disorder in peripheral nerves;
however, a normal control mapmaybe reestablished after section, repair,
and regeneration of sensory nerves of a single finger (Allard et al 1989).
Thus, central corrections mayoccur for the more local disorder in axons
regenerating in a finger.
Evidencefor a limit on the extent of cortical reorganization is seen after
cutting both the ulnar and radial nerves leaving only the median nerve to
the hand (Huerta & Wall 1987). This procedure produces a more extensive
zone of deprived cortex that is not completely reactivated after recovery.
The representation of the median nerve expands over much of the hand
representation, but small zones of Silent cortex remain. Thus, parts of large
zones of deactivation mayremain unresponsive even after long recovery
periods.
Further evidence that the reactivation of cortex is limited by the size of
the deprived zone is seen after cross repair and regeneration of nerves to
the hand (Wall et al 1986, Figure 1H). In this procedure, both the ulnar
and the median nerves are cut, the proximal end of the ulnar nerve is
crossed and sutured to the distal end of the mediannerve, and the proximal
end of the mediannerve tied to prevent regeneration. As a result, the ulnar
nerve regenerates into the skin territory of the mediannerve, and the skin
territory of the ulnar nerve remains denervated. The cross repair results
in islands of cortex in the ulnar nerve zone of area 3b that are activated
by afferents terminating in the skin field of the median nerve. Thus, the
overall cortical mapdoes not reorganize to reflect the altered targets of
the regenerated ulnar nerve (also see Allard et al 1989). Furthermore,
behavioral compensation does not occur, and such monkeyspersistently
mislocalize stimuli on inner to the outer side of the hand. As after median
nerve cut and regeneration, a somatotopically disordered array of reactivated patches of cortex is seen after nerve cross and regeneration. Thus,
local disorder in the regenerated ulnar nerve is not corrected centrally.
Also, eventhoughthe regeneration of the ulnar ncrve is in the skin territory
of the mediannerve, the reactivation is in the cortical territory of the ulnar
nerve. Thus, there is no central correction for the newskin location for the
ulnar nerve afferents. Furthermore, the dorsal hand, which is innervated by
the intact radial nerve, has an expanded representation, indicating the
reorganization of some of the deprived cortex and the formation of a new
activation pattern that is not completely displaced by inputs from the
regenerated nerve. Finally, large zones of silent cortex persist, thus suggesting that the incomplete regeneration of the ulnar nerve together with
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142
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the total lack of regeneration of the median nerve produceda zone of
deprivedcortex that was, as for the two nerve cut preparation, too large
for complete reactivation. However,such zones of silent cortex do not
always occur. In similar experiments, where both the median and ulnar
nerves were cut, no significant zones of silent cortex were observed in
recordings fromarea 3b after a recovery period (Garraghtyet al 1990c).
Reorganization of area 3b has also been demonstratedafter removalof
a single digit in owl monkeys(Merzenichet al 1984, Figure lI). Detailed
microelectrodemapsbefore andweeks after removalof digit 3 at the base,
revealed that the cortical territory normallyactivated by stimulating digit
Figure 1 The reorganization of primary somatosensory cortex (area 3b or S-I proper)
monkeysafter different experimental manipulations. A. The location of area 3b on a dorsolateral view of an owl monkeybrain. Because of the lack of a central fissure, most of the
representation of the body is in the cortex exposed on the surface of the anterior parietal
cortex. The foot and body are represented medially, the hand in the middle, and the face
laterally. B. The topographic order of the hand is largely preserved in the cortex, but the
palmis partially split and the dorsal surfaces of the hand and digits are largely split to medial
and lateral cortical locations (shading). Digits and pads are traditionally numbered, and
insular, hypothenar, and thenar pads are lettered. C. The representation of the hand is
distorted in shape to fit a rectangle of cortex, digit tips occupythe anterior half of the digit
regions. D. Section or crush deactivates the median nerve and deprives most of the lateral
half (hatched) of the hand representation of normal activation. E. During long-term deactivation of the median nerve by crush or section, the deprived cortex is topographically
activated by stimulating the dorsal surfaces of digits 1-3, and by insular pads and pad 3.
F. After nerve crush and regeneration, a normal mapand even the mapspecific to an individual is recovered. G. After regeneration of a cut and reconnected median nerve, parts of the
deprived territory remain responsive to other inputs, thus indicating incomplete regeneration
and recovery, and parts becomeresponsive to median nerve inputs, but in a somatotopically
disorganized pattern that indicates incomplete compensationfor disorder in the regenerated
nerve. Somerecording sites (dots) have multiple receptive fields. H. After section and suture
of the median nerve to prevent regeneration, and cross suture of the cut ulnar nerve to the
peripheral stump of the median nerve and subsequent regeneration into the median nerve
territory, regions of unresponsive cortex occur as a result of removinginputs from the median
nerve and part of the ulnar nerve. The cortical territory of the ulnar nerve is partly activated
in a somatotopically disorganized mannerby ulnar nerve axons regenerated into the median
nerve skin. Again, somerecording sites have multiple receptive fields. I. After removal of
digit 3, cortex formerly devoted to that digit becomesactivated by the glabrous skin of D2
and adjoining palm. J. Weeksof tactile stimulation of D2 and D3resulted in an expansion
of the tactile representation of D2and D3, especially by increasing the tactile activation of
the adjoining part of area 3a. K. After ablation of the cortex representing D3(left), the lesion
site shrinks over weeks, and some of the sites along the margin of the lesion that were
formerly responsive to D2 and D4 become responsive to D3. L. After a period of hand
use after two digits have been fused, the normally sharp boundaries between the digit
representations are blurred by manyneurons having receptive fields on both fnsed digits. M.
Electrical stimulation of an electrode site in cortex representing D3produces an expanded
zone of cortex with matchingreceptive fields on D3. See text for references.
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PLASTICITY
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’’~
A. ’~
Brain Map
C. Normal
3b {SI Proper)
OF SENSORY AND MOTOR MAPS
~
D. Zone Deprived
by Nerve Section
Map
143
B. Map Somatopic Order
E. Reorganization
after Median N
Section or crush
F. Recovery after
Regeneration
of crushed nerve
C4
H. Altered Recovery
after Regeneration
of Ulnar N. into
Median N. Skin
G. Altered
RecoveryRegeneration
of Cut N.
I. Reorganization
After D3 Ablation
J. Expansion
after D2 & D3
Stimulation
e~D
~
D3
Recovery of
Ablated
Representation
of D3
L. Reorganization
After Digit
Fusion
M. Expansion
After Electrical
Stimulation
e5
I D~
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144
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3 becomesresponsive to light touch on the glabrous surfaces of digits 2
and 4, and to some extent palmar pads.
Theseresults indicate that the same cortical territory can reorganize in
different ways depending on what inputs are removed. After section of the
median nerve subserving glabrous digits 1-3, most of the reactivation is
from inputs from the dorsal surface of the hand, and the cortical territory
of the glabrous surface of I)3 is largely reactivated by inputs from dorsal
skin of D3. After removal of inputs from both the dorsal and glabrous
skin of D3, however, the reactivation of the same cortical zone is from
inputs from glabrous surfaces of D2 and D4. Both inputs from dorsal and
glabrous skin apparently can activate the cortical territory of glabrous I33.
The dorsal D3 inputs may dominate when inputs from the glabrous surfaces of adjacent digits are missing, whereas inputs from glabrous D2 and
D4 may dominate when inputs from dorsal D3 in addition to glabrous D3
are missing.
Effects of Cortical Lesions and Cortical Stimulation
Another way of evaluating the potential of cortical representations to
reorganize has been to ablate all cortex representing somepart of the hand
(see Jenkins & Merzenich1987). Weeksto months after removing all cortex
responsive to light touch on the glabrous surface of D3 in owl monkeys,
somerecording sites in cortex next to the lesion that were formerly responsive to other parts of the hand become responsive to D3 (Figure 1K).
Thus, there was recovery of someof the cortical inputs previously removed
by the lesion. Yet, the amount of cortex activated by inputs from D3
remained small, and larger lesions including the cortex devoted to digits
2-5 were not followed by the recovery of representations of these digits.
The somatotopic mapin area 3b of monkeyscan also be changed, at least
for short periods, by repeated intracortical microstimulation of a given
cortical site (Recanzone & Merzenich 1988). Neurons close to the stimulated site (~ 500 gin) cometo have receptive fields closely matchingthose
of the stimulated neurons (Figure 1M).
Effects of
Changing Skin Stimulation
Patterns
Another way of changing cortical organization has been to fuse the skin
of adjacent digits (Figure 1L; Clark et al 1988). Normally, neurons in
of monkeyshave receptive fields restricted to a single digit. This condition
is changed, however, when the skin of two adjacent digits is fused by
cutting and suturing skin to create a continuous skin surface across the
two digits. Recordings made weeks later from area 3b revealed a number
of receptive fields that bridged the skin of both of the fused digits. This
did not seem to be the result of a mechanical spread of the stimulus or the
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PLASTICITYOF SENSORY
ANDMOTOR
MAPS
145
sprouting of peripheral nerves across digits, since receptive fields remained
on two digits when recordings were made immediately after the digits
were separated. In related experiments, transplantation of skin and its
neurovascular supply from one finger to an adjacent finger in monkeys
appearedto result in a cortical representation of the digits that integrated
the representation of transplanted skin with that of surrounding skin
(Clark et al 1986, also see Merzenichet al 1988). This result is in contrast
to the lack of integration into the larger mapthat is observed after redirection of the ulnar into the mediannerve skin (Wall &Kaas 1986).
Changes in the somatotopic organization of cortical maps of the hand
in monkeysmay also occur as a result of restricted, excessive tactile
stimulation (Figure 1J). Whenmonkeyswere trained to maintain contact
with a rotating disk with one or two digits, there was evidence for an
expansionof the cortical representation of these digits (Jenkins et al 1990).
Muchof this expansion appears to be in the adjoining part of area 3a,
however, which normally is activated largely by deep (muscle) receptors,
but also to some extent, especially for the hand representation, by
cutaneous receptors. Thus, the major effect of the stimulation may have
been to potentiate cutaneous over deep receptor activation.
S-I
OF CATS,
RACCOONS,
RODENTS,
AND BATS
Manyof the studies of cortical mapreorganization have been in S-I of
nonprimates. Someof the earliest studies were on S-I of cats. Raccoons
provide the advantage of studying a large hand area in S-I in which
individual digits are demarcated by shallow sulci. Rats have been useful
in studies in which it is important to study larger numbersof animals or
to have a clear morphological substrate such as the "barrel field." Bats
provide an opportunity to study a cortex in which the representation of
the forelimb is quite different.
The Effects
of Removing Peripheral
Inputs
The results of several studies on nonprimates are in agreement with those
on monkeysthat show that cutting a peripheral nerve or removing a skin
field alters the cortical map; the deprived cortex in S-I is not permanently
deactivated, but it becomesresponsive to remaining inputs. In an early
landmark study, Kalaska & Pomeranz (1979) reported that several weeks
after section of the nerves to the forepaw in adult cats, cortex formerly
responsive to the forepaw became responsive to the normally innervated
forearm (however, the change was more impressive in kittens). Similarly,
when the hindlimbs and tails of cats were deafferented by selectively
sectioning dorsal roots entering the spinal cord, portions of $-I normally
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146 I~,As
representing these body parts were activated by stimulating the abdomen,
thorax and forelimb, and no silent cortex was observed (Franck 1980).
Earlier, Metzler & Marks (1979) had shown that such changes in S-I can
be quite rapid by recording from neurons formerly responsive to the upper
hindlimb after reversal blocks of inputs from the upper hindlimb produced
by injections of local anesthetic. While most recorded neurons in the cortex
for the upper hindlimb could not be driven after the block, over a quarter
of the sampled neurons immediately acquired new receptive fields on the
hindpaw or abdomen. More recently, Brandenberg & Mann (1989) have
recorded from the forepaw cortex in S-I of cats weeks after crush and at
least partial regeneration of the sensory nerves to the skin of the forepaw.
This procedure revealed a small proportion of abnormal neurons that
responded to stimulation of the hindpaw as well as the forepaw, thus
suggesting that someeffects of reorganization as a result of denervation
can persist for sometime after reinnervation. Finally, the removal of a
forepaw digit in adult cats is followed by a dramatic expansion of the
representations of adjacent digits in contralateral S-I when measured by
the 2-deoxyglucose technique for revealing metabolically active cortex
(Juliano et al 1990).
Removinginputs at a higher level by damaging the spinal cord may
produce somatotopic reorganizations in S-I of cats as well. In an early
study, Levitt & Levitt (1968) reported that the responsiveness of the
hindlimb cortex of adult cats to low-threshold cutaneous stimuli was
abolished by lesions of both the contralateral dorsal and lateral columns,
although the topography of cortex subserved by inputs above the lesion
was unchanged. McKinley et al (1987) recently demonstrated, however,
that after deactivation of the hindlimb cortex of S-I by lower spinal cord
transections in kittens, this cortex ultimately becomesresponsive to the
trunk. Reactivation of deprived cortex was more extensive in kittens sectioned at 2 weeks than 6 weeks of age, but the magnitude of the changes
that occurred after the sections at 6 weeks of age suggests that some
plasticity could follow such sections in adult cats.
Alterations produced by digit removal have been extensively investigated in raccoons. These carnivores have the advantage of a large representation of the glabrous forepaw that is separated from other parts of
S-I by the fusion of the coronal and postcruciate fissures (Welker
Seidenstein 1959). Furthermore, spurs on the triradiate sulcus separate
palm and digit representations, and digit 2 and 3 representations, and
cortical dimples mayindicate further divisions. Thus, the locations of the
representations of individual digits and pads of the forepawcan be closely
approximated from surface landmarks.
The first experiments were on the long-term effects of digit removal in
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PLASTICITY
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AND MOTOR MAPS
147
young, 2-8-week-old raccoons, and the reactivation of the deprived cortex
by inputs from adjoining digits and parts of the palms was observed
(Kelahan et al 1981). Subsequent experiments demonstrated a similar reorganization of S-I after removalof digits in adult raccoons. The immediate effect of removing digits in adult raccoons appears to be a profound
deactivation of the cortex for that digit. On the same day of amputation,
Rasmusson& Turnbull (1983) found that responsiveness in the deprived
cortex to adjacent intact digits was largely restricted to responsiveness to
the offset of skin indentation, presumablyas a result of the offset of inhibition generated by the stimuli. In similar experiments, however, Kelahan
& Doetsch (1984) found that some neurons in the deprived zone
cortex were immediately activated by low-intensity stimulation of adjacent
digits. A consistent finding was that over several weeks, the deprived cortex
becamehighly responsive to light cutaneousstimuli on the digits next to the
removed digit (Rasmusson 1982, Rasmusson & Turnbull 1983, Kelahan
Doetsch 1984). An even more dramatic reorganization of S-I cortex was
reported for a raccoon that had been caught in the wild at some unknown
length of time after the loss of a forepaw (Rasmusson et al 1985).
this raccoon, recording sites throughout the forepaw region of S-I were
responsive to stimuli on the forelimb stump, and somesites were responsive
to tactile stimulation of the glabrous hindpaw. These observations raise
the possibility that the entire, quite large forepawarea of S-I in adult
raccoons can reorganize and becomeresponsive to other inputs. Another
possibility is that someor muchof the reactivation was from persisting
forepaw nerve terminations in the stump.
Cortical reorganization has been studied in S-I of adult rats after section
of the sciatic nerve (Wall &Cusick 1984), after a cytotoxin has been used
to kill primary neurons in the sciatic nerve (Wall et al 1988), and after
denervation of a row of mystacial vibrissae follicles (Welkeret al .1988).
In normal rats, about 85%of the hindpaw representation depends on the
sciatic nerve and 15%on the saphenous nerve. After section of the sciatic
nerve, the representation of the saphenous nerve expanded about three
times in surface area into, but not completelyfilling, the territory of the
sciatic nerve. The expansion occurred rapidly, within 1 or 2 days, and
remained stable for at least several months; however, about half of the
total hindpawrepresentation remained unresponsive to cutaneous stimuli.
The removal of sciatic nerve neurons with the toxin, ricin, produced a
nearly identical result. Since most dorsal root ganglion cells in adults
survive peripheral nerve section, maintain central connections in the spinal
cord and dorsal column nuclei, and have some level of spontaneous
activity, these experimentsindicate that the presence or absence of sciatic
nerve terminals is not a major factor in determiningthe extent of plasticity.
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148
KAA$
Microelectrode recordings of the lace representation in S-I o1" adult mice
(Wetker et al 1988) and 2-deoxyglucose measures of metabolic activity
adult rats show that representations oI ~ normally innervated vibrissae
expandinto the cortical territories of denervated vibrissae within months
after deactivation (Kossut et al 1988, Kossut 1988).
The effects of amputating a body part on S-I organization has also been
studied in an Australian fruit bat, the flying fox (Pteropus). Thoughmost
of the forelimb digits have been modified to support the wing membrane,
the first digit protrudes from the wing and is used for climbing. In normal
bats, DI has a large representation in caudal S-I (Calford et al 1985).
Weeksat’ter amputation or" D1, recordings in the deprived cortex, where
neurons previously had receptive fields restricted to D 1, reveal newreceptive fields that include the skin of the intact adjacent wrist and metacarpals,
and the adjacent wing membrane (Calford & Tweedale 1988, 1990).
Immediately after the amputation, the deprived cortex was silent, but
within 20 h, responsiveness returned and the deprived neurons had large,
new receptive fields. Over a period ot" days, however, the new receptive
fields becamemorerestricted in size.
Peripheral denervations in adult mammalsnot only produce reorganizations in somatotopyin S-I, but also alter the expression of inhibitory
neurotransmitters and levels of metabolic activity. Lesions of the follicles
of mystacial vibrissae in rats and mice are followed in days by a decrease
in the deprived cortex in the expression of the inhibitory neurotransmitter,
GABA,that lasts for weeks (Welker et al 1989). Reductions in the
expression of the metabolic enzyme, cytochromeoxidase, also occur in the
deprived cortex (Wong-Riley & Welt 1980). Such lesions also produce
increases of about 40%in the sizes of metabolically active columns of
tissue in S-I for adjacent vibrissae as revealed by 2DGuptake (Kossut et
al 1988; also see Melzeret al 1989).
Reorganization
of S-I Following
Peripheral
Stimulation
There is someevidence that increasing the activity in peripheral nerves
increases the extent of the cortex activated by these inputs. In an early
report, Spinelli &Jensen (1979) recorded from the cortex in kittens that
had received avoidance training by shocking one forearm in a daily session.
Spinelli & Jensen noted that the representation of the t’orearm was many
times larger in S-I contralateral than ipsilateral to the shockedforearm.
While the effects were attributed to changes in brain development,similar
effects mayoccur in adults. Morerecently, Recanzoneet al (1990) reported
that a single session of 6-8 hours of electrical stimulation of a cutaneous
nerve in adult cats is rapidly t’ollowed by at 1cast a short-term expansion
of the cortical representation of that nerve. After periods of stimulation
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PLASTICITYOF SENSORY
ANDMOTOR
MAPS
149
of pairs of mystacial vibrissae in rats, neuronsin S-I enlarge their receptive
fields to include both whiskers (Yun et al 1987, Delacour et al 1987).
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REORGANIZATION
OF
AREAS IN PRIMATES
HIGHER
CORTICAL
After sources of input have been removed, somatotopic reorganizations
have been observedin area 1 of anterior parietal cortex and S-II of lateral
parietal cortex of monkeys. Area 1 was once included with area 3b and
other areas in a large "S-I" (see Kaas 1983 for review). It is nowclear,
however, that both areas 3b and 1 contain separate, congruent, and parallel representations of cutaneous receptors in a manneranalogous to V-I
and V-II of visual cortex. Though both areas 3b and 1 receive direct
input from the ventroposterior nucleus, the input to area 1 is sparser and
from thinner axons and axon branches. Area 1 receives its major feed
forward inputs from area 3b. Lesions of area 3b deactivate area 1, but
lesions of area 1 do not deactivate area 3b (Garraghty et al 1990b).
Thus, area 1 can be considered as a higher somatosensory area than
area 3b.
Although area 1 has not been as extensively studied as area 3b after
peripheral nerve manipulations, the normal dependencyof area 1 activity
on area 3b suggests that all changesobserved in area 3b should be reflected
by similar changes in area 1. This assumption appears to be largely supported. Thus, nerve section produced somatotopic reorganizations in both
areas 3b and 1 of monkeys(Merzenich et al 1983a), and nerve section,
repair, and regeneration resulted in similar mixtures of reorganization and
disorderly reactivation in both fields (Paul et al 1972, Wall et at 1986). The
details of the topographical transformations that were produced were
different in areas 3b and 1 in both types of experiments, however, and
these differences were interpreted as evidence that somereorganization
occurs within area 1. Thus, area 1 reorganization mayreflect both relayed
and intrinsic plasticity.
More recently, major somatotopic changes have been reported for
S-II of macaquemonkeysafter partial lesions of area 3b and adjoining
somatosensoryfields of the anterior parietal cortex. $-II receives dense
inputs from all anterior parietal fields, and sparse inputs from the ventroposterior nucleus of the thalamus (see Kaas & Pons 1988 for review).
S-II is completely dependent on anterior parietal cortex, probably from
both direct and indirect inputs from area 3b, for activation by cutaneous
stimuli (Pons et al 1987, Garraghty et al 1990c, Burton et al 1990). Thus,
lesions of the anterior parietal cortex that removecortex representing the
hand in areas 3a, 3b, and 1 and 2 abolish all activation of neurons in S-II
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150
KAhS
.by stimulation of the hand. Indeed, the cortex normally responsive to
stimulating the hand in S-II is initially unresponsive to the stimulation of
any body part after the lesion. Recordings made weeks after the lesion,
however, reveal a complete recovery of responsiveness in the deprived
cortex to stimuli to other parts of the body, largely the foot (Pons et al
1988; Figure 2).
These results provide compelling evidence that somatotopic changes do
occur in the cortex, and are not solely relayed from subcortical structures.
It seems unlikely that the cortical lesions produce subcortical plasticity
that is somehowrelayed to S-II. Rather, changes in the effectiveness of
connections in S-II from anterior parietal cortex wouldbe the likely source
of the reactivation. The results also suggest that higher cortical stations
have greater potential for plastic changes than lower stations. Whentwo
nerves are cut or damagedto denervate most of the hand, parts of the
representation of the hand in areas 3b and 1 may not recover responsiveness to cutaneous stimuli (e.g. Wall &Kaas 1986, Huerta &Wall 1987).
Removingall of the inputs from the hand by cortical lesion, however, is
followed by complete reactivation of S-II. Possibly, higher stations such
as the parietal ventral area (Krubitzer & Kaas 1990) have even more
potential for reorganization.
SOMATOTOPIC
SUBCORTICAL
REORGANIZATION
LEVELS
AT
Twoextreme positions are (a) that all reorganization in the somatosensory
systemoccurs at the cortical level, and (b) that all changesin cortex reflect
alterations relayed from subcortical levels. This review is largely concerned
with cortical maps, because changes can be more clearly demonstrated in
these larger, more accessible, two-dimensionalrepresentations, and any failure to find evidence of mutability at cortical levels would suggest that
looking at subcortical levels wouldbe unrewarding. The reviewed evidence,
however, strongly suggests that plasticity occurs at both cortical and
subcortical levels.
There have been some questions about the existence of somatosensory
reorganization in the spinal cord of adult mammals.Peripheral afferents
enter the spinal cord and terminate in the dorsal horn or in the lower brain
stem, where they form somatotopic representations. The possibility of
extensive reorganization of the map in the spinal cord of adults was
suggested by early evidence for collateral sprouting of intact inputs into
regions of the spinal cord of cats deprived by partial denervation (e.g. Liu
& Chambers 1958). Researchers using current techniques have failed to
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A.
151
LOCATION OF ANTERIOR PARIETAL FIELDS
3a, 3b,IAND2AND Sit IN MACAQUE MONKEY
Opened Lateral
B.
SulcuS
CORTICAL LESION
Tr
C.NORMAL SII
Unkr.~_~
Figure 2 The second somatosensory area, S-II, depends on inputs from representations in
the anterior parietal cortex, largely area 3b, for activation, Thus, a lesion of the hand
rel~resentations of the anterior parietal cortex (areas 3a, 3b, 1 and 2) deactivates the hand
region of S-If, which becomesresponsive to the foot. A. The locations of S-II in the opened
central and lateral sulci of a macaquemonkey.B. A strip lesion of hand cortex deactivates
the hand region of S-II. C. The normal mapof the contralateral body surface in S-II. D. The
altered mapsmonths after lesion of anterior parietal cortex, Based on Pons et al (1988).
Figure reproduced from Kaas & Garraghty (1989).
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152
KAAS
demonstrate such sprouting (e.g. Rodin & Kruger 1984), however, and
alternative explanations of pre,vious results have been offered (see Pubols
&Bowen1988 for review). Yet, the lack of convincing evidence for sprouting
does not mean that reorganization does not occur by other means, and
the electrophysiological evidence for plasticity seems more compelling.
The immediate effect of denervation by nerve cut or section of dorsal
roots seems to be to completely deactivate neurons with receptive fields in
the denervated skin (Wilson & Snow1987, Pubols & Goldberger 1980,
Brownet a11984, Devor & Wall 1978, Lisney 1983, Pubols 1984). Evidence
has been presented for rather extensive reorganization in the dorsal horn
after weeks of recovery (Basbaum& Wall 1976, Devor & Wall 1978, 1981),
but such changes have not always been reported (Brownet al 1984). Recent
reports describe a more limited spatial reorganization in the spinal cord
that is restricted to the formation of newreceptive fields very close to the
original receptive fields (Wilson &Snow1987). These authors conclude
that the magnitudeof the change is so small that it wouldbe easily missed
in most experiments.
There have been only a few experimental investigations of plasticity in
the dorsal column-trigeminal complex after peripheral nerve injuries in
adult mammals.Miller et al (1976) reported that cutting all but one of the
dorsal roots related to the hindlimb in cats immediately deactivated many
neurons in the gracile nucleus. Theyobserved an increase in the size of the
representation of the intact root after months of recovery, however, and
fewer nonresponsive neurons. Whenall the dorsal roots for the hindlimb
were cut (Dostrovsky et al 1976), the immediateeffect was an increase
the number of neurons with receptive fields on the abdomen.Furthermore,
someof the neurons with receptive fields on the leg acquired new receptive
fields on the abdomenduring a reversible cold block of the afferents from
the hindlimb. More recently, Kalaska & Pomeranz(1982) studied kittens
weeks after forepaw denervation and found that in the dorsal part of the
cuneate nucleus, where neurons normally have receptive fields on the
forepaw, manyneurons had receptive fields on the wrist, forearm, or trunk.
These experiments indicate that some degree of somatotopic reorganization occurs in the dorsal columnnuclei after peripheral injury or deactivation, and that changes can be quite rapid. However,reorganization maybe
quite limited or absent in somecircumstances. Waite (1984) reported that
2 monthsafter section of the infraorbital nerve to whiskers in adult rats,
there was no evidence for plasticity in the trigeminal nhclei.
Somatotopic plasticity has also been reported for the ventroposterior
(VP) nucleus of the thalamus of adult rats and cats after the partial removal
of inputs. In an early landmark study in adult rats, Wall & Egger (1971)
ablated muchor all of the gracilis nucleus, which represents the hindlimb,
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PLASTICITY OF SENSORY AND MOTORMAPS
153
and found no immediate somatotopic change in the VP. Yet recordings
one week or more after the lesion provided evidence for an expansion of
the forepaw into the hindpaw representation, and the authors concluded
that thalamic cells projecting to hindlimb cortex had acquired new receptive fields on the forepaw. The reported expansion was small, however, on
the order of a 200/~mor less. Thus, it would be useful to look for the
relay of such proposed changes by recording from primary somatosensory
cortex, where the forepaw and hindpaw are represented in quite separate
locations. In monkeys,section of the dorsal columninput to the gracilis
nucleus was followed by an expansion of the forelimb representation into
the most lateral part of the VP, wherethe hindlimb is normally represented
(Pollin & Albe-Fessard 1979). Even earlier evidence for somatotopic
change stems from studies showing that the receptive fields of some
neurons in the VP can immediately change from one skin location to a
nearby location where the skin region of the original receptive field is
anesthetized by subcutaneous injections of procaine (Nakamaet al 1966).
More recently, extensive reactivation of the hand subnucleus of VP by
inputs from the dorsal hand was found in squirrel monkeyswith chronic
section of the median and ulnar nerves to the glabrous hand (Garraghty
et al 1990a).
REORGANIZATION
REPRESENTATIONS
OF
VISUAL
Although the organization of the visual cortex has been considered to be
highly stable in adult mammals,recent evidence indicates that considerable
retinotopic reorganization can occur as a result of removing someof the
retinal inputs. In mammalswith frontally directed eyes, most visual areas
can be activated by retinotopically matched inputs from either eye. In
adult cats, parts of primary (V-I or area 17) and secondary (V-II or area
18) visual cortex were completely deprived of their normal sources of
activation by removingone eye, and placing a 5-10° lesion near the central
vision in the retina of the remaining eye (Kaas et al 1990). By itself,
lesion of the retina had little impact on the retinotopic organization of
visual cortex. Recordings in rows of electrode penetrations across cortex
producednormal sequences of receptive fields for each eye until the region
of the cortex deprived by the lesion was encountered. Then, neurons only
respondedto the intact eye, since retinotopically matchingreceptive fields
wouldbe in the location of the retinal lesion. Whenrecordings were made
weeksafter thc removalof onc eye andthe placing of a small lesion in the
other eye, the receptive field progressions indicated that the retinotopic
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154
organizations of both V-I and V-II were altered. Recordings outside the
deprived zone of cortex produced normal progressions of receptive fields
for the remaining eye. In contrast, recordings in the binocularly deprived
zone of cortex revealed that neurons had acquired new receptive fields that
were displaced from expected locations in the lesioned part of the retina
to intact parts of the retina aroundthe lesion (Figure 3). The reorganization
was not retinotopic, in that the newreceptive fields did not form retinotopic
progressions. Rather, neurons across 2-3 mmof cortex typically had
similar, highly overlapping receptive fields in a part of the retina next to
Left Visual Hemifield
°10
VM
o
S
o
5
.M I
I
Lesion
area 17
Cat Brain
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PLASTICITY OF SENSORY AND MOTORMAPS
155
the lesion. In addition, neurons in adjacent recording sites in the deprived
zone of cortex sometimeshad quite separate receptive fields on opposite
sides of the lesion. A few recording sites were activated from locations on
both sides of the lesion. Althoughthe extent of the reorganized cortex was
°,
large, as much as 4-6 mmin width, larger retinal lesions of 10-15
depriving an even larger zone of cortex, produced a fringe of deprived
cortex with reactivated neurons and new receptive fields, and a central
core of silent cortex where neurons were not driven by visual stimuli.
Comparable results were obtained in a monkeywhere matching lesions
were placed in the fovea of each eye (Heinen &Skavenski 1988). Neurons
in V-I initially unresponsive to visual stimuli later became responsive.
These observations, though quite limited in extent, are important in that
they indicate that the visual cortex, like the somatosensory cortex, is
capable of reorganizing as a result of restricted deprivations to create new
representations of receptor surfaces.
Other evidence for the reorganization of the visual cortex after partial
deprivation stems from experiments on cats in which the optic chiasma
was sectioned (Milleret &Buser 1984). This procedure produced a decrease
in average receptive field sizes in area 18 (V-II) of cats by removing
activation from the ipsilateral temporal retina. Over a period of weeks,
however,neurons in area 18 progressively recovered large receptive fields,
but only if visual experience was allowed. In another type of experiment
(Krubitzer & Kaas 1989), partial lesions of area 17 in owl monkeyswere
found to deactivate a part of the middle temporal visual area, MT, which
receives direct inputs from area 17. Recording immediately before and
Figure 3 The reorganization of the visual cortex after retinal lesions in cats. A region of
primary visual cortex (area 17) was deprived of its normal sources of visual activation
removingthe ipsilateral retina and placing a 5° lesion in the retina of the contralateral eye.
Rowsof recording sites (such as row A 1-5 on the lower right) outside the deprived zone
cortex producednormal progressions of receptive fields in the contralateral visual hemifield
(A 1-5, upper). Rowsof recording sites across the deprived zone (such as row B 1-5) would
normally produce similar progressions of receptive fields corresponding to the lesioned
portion of the retina. Instead, receptive fields cluster around the margins of the lesion (or
the projection of the lesion into the visual field), and somerecording sites produce split
receptive fields on opposite sides of the lesion (B1). A dorsal view of the cat brain on the
lower left showsthe location of area 17 in the right hemisphere. Anenlargement of a portion
of cortex indicates recording sites in area 17, including a portion schematically unfolded
from the medial wall of the hemisphere. The lon.q dashed line marks the lateral border of
area 17 correspondingto the zero vertical meridian (line of decussation), and the short dashed
line marks the zero horizontal meridian separating the rostral representation separating the
rostral representation of the lower visual quadrant from the lower representation of the
upper visual quadrant. Recordings in area 18, the second visual area, revealed a similar
reorganization. Based on Kaas et al (1990).
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156
KAAS
after the lesion revealed a narrow fringe of cortex around the deactivated
zone in MTwhere neurons could be activated, but had slightly displaced
receptive fields that correspondedto parts of the retina still represented in
area 17. In related experiments in macaquemonkeys, Dwayneet al (1987)
recorded from neurons in MTbefore and over days after a partial lesion
of MT,and found a scattering of neurons with expanded receptive fields.
After lesions of the retina, retinotopic changes similar to those observed
in the cortex, but of lesser magnitude, have been reported for the lateral
geniculate nucleus (Eysel et al 1980, 1981, Eysel 1982). Small, 3-4° lesions
placed in the paracentral retina of adult cats completely deactivated a
narrow column of neurons in a layer of contralateral LGN.After 1 month
or more of recovery, however, such neurons regained excitability to visual
stimuli within receptive fields displaced from the region of the lesion to
the immediate surround of the lesion. The spread of excitation into the
deactivated projection column in the LGNwas estimated to be of the
order of 100-200 #m. Lesions producing larger zones of deactivation
resulted in a persistence of unresponsive neurons, except at the border of
the deprived zone.
REORGANIZATION
OF AUDITORY CORTEX
The possibility of reorganization of auditory cortex has been investigated
recently by placing small unilateral lesions in the cochlea of adult guinea
pigs (Robertson & Irvine 1989). Guinea pigs have two tonotopically organized areas in auditory cortex that have been termed the caudal and rostral
fields (Robertson &Irvine 1989) because homologies between these fields
and the primary field A-I and the primary-like field R (rostral) of primates
and squirrels and A (anterior) of cats remain uncertain (see Luethkeet
1988 for review). Immediately after the cochlear lesions, neurons within
the deprived isofrequency bands in the rostral field were depressed, but
could be activated by more intense tones of frequencies spared by the
lesion (increases of 30+ dB). After one month or more, neurons in the
deprived cortex had response thresholds that were close to normal for
sound frequencies adjacent to the frequency range damagedby the lesion.
Morelimited results suggested that a similar change occurred in the caudal
auditory field. Thus, the auditory cortex of adult mammals
has the capacity
to expand the representations of sound frequencies related to intact portions of the cochlea into zones of cortex deprived of normal sources of
activation by cochlear damage(Figure 4). Such potential for reorganization apparently exists in at least two auditory fields (also see Weinberger
& Diamond 1987).
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PLASTICITY OF SENSORY AND MOTORMAPS
157
Brain
KHz
__ High
’,1
deprived
k } ~ Cochlea lesion
bylesion
v ~
IOKHz
Fi#ure 4 The reorganization of auditory cortex after partial lesions of the cochlea. Lesions
of a part of cochlea devoted to a restricted range of auditory frequencies deprived a zone of
the contralateral auditory cortex of its normal source of activation. Initially, neurons in the
deprived zone had greatly depressed responsiveness to auditory stimuli, but over one month
or more, these neurons became highly responsive to frequencies represented in adjoining
isofrequency bands. The location of the auditory cortex is shownon a dorsolateral view of
the guinea pig brain above. Recordings were from a rostral auditory field that is primarylike, and maybe A-I (see text). Reorganization was also noted in an adjoining posterior
auditory field. Normal "A-I" is depicted on the lower left, which shows a rostrocaudal
progression of the representation of low-to-high frequencies and the dorsoventral course of
isofrequency lines. Frequency change is gradual rather than stepwise as shown. A cochlear
lesion produces a profoundly deprived zone of cortex, which is later activated by inputs from
adjoining intact portions of the cochlea, as shownin the lower ri#ht. Based on Robertson &
Irvine (1989).
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158 r~AAS
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REORGANIZATION
OF MOTOR CORTEX
The motor cortex of mammalsincludes a primary field, M-I, and typically
several other motor fields. Systematic mapsor representations of motor
movements have been demonstrated in M-I of rats and other mammals
by electrical stimulation; the most detailed maps are produced by low
levels of current passed through the tip of microelectrodes that penetrate
to the deeper layers of cortex. Although strong or repetitive electrical
stimulation of the cortex can alter the types of movementsproduced at
cortical sites (e.g. Nudo& Merzenich 1987, Brown& Sherrington 1912),
thereby demonstrating a form of plasticity in the motor cortex of adults,
the mapcan be quite stable over time whennear-threshold levels of stimulation are used (Craigs &Rushton 1976). Nevertheless, recent experiments
have shownthat the portions of M-I of adult rats can change if parts of
final motor pathways are eliminated (Donoghueet al 1990, Sanes et al
1988, 1990). In these experiments, sectioning of a motor nerve to muscles
of part of the body or the removal of a part of the body have been
used to eliminate the possibility of movementfor these body parts. The
immediateeffect in cortex was that the stimulation of sites that formerly
moved the inactivated or removed body part no longer produced movements.
Withinhours of the lesions, however,stimulation of these sites resulted
in the activation of new sets of muscles (Figure 5). For forelimb amputations, representation of the shoulder in M-I enlarged. After section of
the branches of the facial nerve that innervate the musculature for the
facial vibrissae, the representations of both the eyelid and eye and the
forelimb regions enlarged.
MECHANISMS OF REORGANIZATION
The two main mechanisms proposed for the observed changes in sensory
and motor maps have been the growth (collateral sprouting) of new connections and alterations in the effectiveness of previously existing connections by forming new synaptic contacts or potentiating existing synapses (see Wall 1977, Devor &Wall 1981, Kaas et al 1983, Pearson et al
1987, Wall 1988). Since manyof the changes are quite rapid, over hours
to days, most investigators favor the interpretation that at least these early
changes are the result of potentiating previously existing connections. This
interpretation seems possible in that the magnitudesof the cortical changes
are often, but not always (e.g. see Rasmusson& Nance 1986), within the
extents of individual thalamocortical axons, which can be 1 mmor more
in width (e.g. Landry et al 1982, Florence &Casagrande 1987, Garraghty
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PLASTICITY OF SENSORY AND MOTORMAPS
¯
normal
159
~
weeks
Facial nerve section
Figure 5 Reorganization of the primary motor cortex (M-I) after section of the facial nerve
to the musculature of the facial vibrissa. Adorsolateral view of a rat brain above showsthe
locations of the primary somatosensory (S-I) and motor (M-l) areas. The normal organization of the motor mapis approximatedon the lower left. Weeksafter section of branches
of the facial nerve that innervate the vibrissa, electrical stimulation of cortex formerly devoted
to producing movementsof vibrissa, instead produced eye and eyelid as well as forelimb
movements. Thus, the effective eye and forelimb regions of M-I that were enlarged into
vibrissa cortex deprived by inactivation of the effectors. Other experimentsinvolving forelimb
amputation enlarged the representation of shoulder movements.Based on Sanes et al (1990).
N, neck; Tr, trunk.
et al 1989). Furthermore, somatotopically "inappropriate" projections of
thalamic neurons with receptive ficlds on one toe to cortex representing
another toe have been demonstrated electrophysiologically in cats (Snow
et al 1988). Thus, expansions of representations could occur simply by
extending the activating effectiveness of synapses from the dense core to
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160
KAAS
the sparse fringe within the terminal arbors of axons when the fringe
extends into the deprived zone of cortex. Of course, lateral intrinsic connections within representations, which can be quite extensive (e.g. Rockland & Lund 1982, DeFelipe et al 1986), could also increase the zone of
effective spread, and changes relayed from one to the next level in a
cascading fashion could ultimately becomevery extensive. In addition, the
dendritic branches of individual neurons can extend over hundreds of
microns. Finally, at least some structures appear to have maps of inputs
that are normally subthreshold or unexpressed, but they maygain potency
when the inputs of the dominant map are removed (see Rhoades et al
1987). Thus, existing connection patterns are widespread enough to be
compatible with the extents of most or all observed reorganizations. The
growth of axons (see Goldberger 198 l) and dendrites (see Purves &Hadley
1985) may indeed contribute, but such growth may not be of enough
magnitudeto be the major factor in the reorganization of brain maps (see
Rodin & Kruger 1984, Rodin et al 1983, Stelzner & Keating 1977, Baisden
et al 1980, Rasmusson & Nance 1986, Rasmusson 1988).
A number of ways of increasing synaptic effectiveness have been postulated (e.g.Wall 1977, Wall et al 1989a). An immediate enhancement
previously existing excitatory pathways mayresult by the deactivation of
tangentially spreading inhibitory connections, while other, more slowly
developing potentiations mayfollow the reduction of inhibition as a result
of activity-dependent regulation of neurotransmitters and metabolic
enzymes. For example, nerve section (Garraghty et al 1990a) and eye
removal (Hendry &Jones 1988) reduce the expression of GABA
in cortex,
and presumably increase the excitability of neurons (see also Dykes et
al 1984). The renewal of synaptic boutons is a feature of reorganizing
cortex after lesions (see Ganchrow&Bernstein 1981), and alterations
synapse shape, number, size and type maybe important in mapplasticity
(Greenough & Chang 1985; Markus & Petit 1989). The blocking
retinal impulses in adult monkeysappears to induce changes in neuronal
structure and synapses in visual cortex (Wong-Riley ct al 1989), and
removing thalamic projections to motor cortex is followed by an increase
in synapses related to previously existing inputs from parietal cortex
(Ichikawa et al 1987).
Anotherfeature of reorganization is that it sometimes, but not always,
appears to be topographic. The changes described in the visual cortex
appear to be simply of reactivation without retinotopic remodeling, and
the reactivation of digit cortex in raccoons does not create a somatotopic
order within the reactivated zone. However, months after digit removal
(Merzenich et a11984) or nerve section (Merzenich et a11983a) in monkeys,
there is evidence for the presence of topographically ordered represen-
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PLASTICITY
OF SENSORY AND MOTOR MAPS
161
tations of preserved inputs in the deprived cortex. The emergenceof such
order could require factors in addition to the increases of effectiveness of
previous connections as a result of the deactivation of alternative inputs.
Thus, theories of synapse selection based on coactivation and competition
have been proposed as mechanisms for topographic "self-organization"
(see Willishaw &vonder Malsburg 1976, Pearson et al 1987, Merzenich
1987).
Recent research suggests a role for the excitatory aminoacid receptor,
N-methyl-D-aspartate (NMDA)
in cortical reorganization (see Cotman
al 1988). The NMDA
receptor appears to regulate the flow of calcium ions
into neurons, and the presence of calcium maybe a factor in strengthening
synapses. The NMDA
receptor has been implicated in use-dependent
developmentplasticity in the visual cortex (Gruel et al 1988, Kleinschmidt
et al 1987, Bear et al 1987), and the receptor mayhave a similar role in
adult plasticity.
CONCLUSIONS
The reviewed research supports a number of conclusions on the nature
and extent of reorganization of sensory and motor mapsin adult mammals.
1. Reorganization of sensory maps follows changes in neural activity
patterns induced by the relative inactivation of feedforward pathways
producedby lesions or removals of sensory surfaces, peripheral nerves,
or more central structures. Motor maps reorganize by changing the
effectiveness of outputs to remaining effectors whenthe access to the
preferred effectors is blocked by removalor lesions.
2. Increases in the relative activity of parts of pathwaysin a sensory system
can increase the sizes of the representations of those parts in central
maps. Alterations are produced by both sensory and electrical stimulation.
3. Ablation of parts of representations can be followed by partial or
complete recovery of those parts in reorganized representations.
4. Reactivation sometimes, but not always, creates a topographic pattern.
5. Sensory mapsboth early and late in processing hierarchies are mutable,
but changes are more dramatic in higher stations, possibly because of
the accumulationof serial changes and greater potential for plasticity.
6. Sensory maps in the somatosensory, visual, and auditory systems are
capable of change.
7. Sensory maps in a range of mammalianspecies have been shown to
change. The clear implication is that adult plasticity is a feature of all
mammalian brains.
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8. Somechanges are so rapid, within hours, that the potentiation and
modification &existing synapses rather than growth of new connections
is the likely explanation. Since other modifications appear to take place
over longer periods of weeks and perhaps months, sprouting of central
axons maybe an additional factor, but clear experimental evidence is
needed. Sprouting maybe muchmore significant in developing brains.
The emergence of topographic features in some reorganizations may
depend on synapse selection based on competitive interactions and
temporal correlations and discorrelations in neural activity.
9. There is presently little evidence related to the behavioral consequences
of mapreorganization, if any, but partial recoveries of lost abilities
following central damageand improvementsand alterations in sensory
and motor skills are possibilities (see Merzenich et al 1988, Wall
Kaas 1985).
ACKNOWLEDGMENTS
I thank P. E. Garraghty and S. L. Florence for commentson the manuscript.
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