ARTÍCULOS DE REVISIÓN
The 47,
The hand and the brain
G. Lundborg
Department of Hand Surgery, Malmö University Hospital, Sweden
Correspondencia:
G. Lundborg
Department of Hand Surgery, Malmö University Hospital, Sweden
SE 20502 Malmö. Sweden
(goran.Lundborg@hand.mas.lu-se)
Everyone involved in hand surgery and hand rehabilitation
is well aware of the importance of well functioning hands for
our patients’ well being and life quality. A powerful pain free
handgrip and well-coordinated precision movements of the fingers
together with well-preserved sensory functions form a base for
every individual’s working capacity. Our hands are heavily involved
in the interaction with other individuals in social life. Impaired
hand function may have serious consequences for activities of
daily living as well as subjective well being of our patients.
The outer brain
The philosopher Descartes named the hand the outer
brain – a very clever expression for the close and intimate
interaction between the hand and the brain. The hand is – like
the brain – intelligent, it remembers, and it can improvise. The
hand can be regarded an extension of the brain to the
environment. Through the sense of touch our hands helps to
explore and perceive the surrounding world. The hand is a symbol
for identity and is intimately linked to our personality. The
movements and gestures of our hands are important components
of the body language, helping to express our feelings and being
an important tool for communication with other individuals.
The touch of a hand generates comfort and consolation. In
fact, the pleasant feeling of well being which is generated by
the touch of hands has recently been linked to a special system
of small-sized nerve fibres – producing a faint sensation of
pleasant touch. fMRI analysis during stimulation of these C tactile
afferents in hairy skin showed activation of the insular region of
the brain but not of somatosensory areas S1 and S2 (Olausson
et al., 2002). The findings identify these C tactile afferents as
a system for limbic touch that may underlie emotional, hormo-
nal and affiliative responses to caress-like, skin-to-skin contact
between individuals.
The sense of touch
The sensibility of the human hand is extremely well
developed and essential for hand function. Protective sensibility
is necessary to avoid injuries to the hand (Brand and Yancey,
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hand2003,
and the
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1993). Stereognosis, the functional sensibility of the hand also
called tactile gnosis, makes it possible to recognise and identify
textures and shapes. The hands are our eyes in darkness helping
to create an inner picture in our mind of the structures, textures
and items which are touched. Blind people use the sense of
touch in their fingertips for replacing vision when reading in
Braille. Hands are sensitive and respond to vibrations, and it is
well known that deaf people can sometimes listen with their
hands. One of the viola players in the London symphony orchestra
became gradually deaf during the teen ages. Although she can
not hear music she feels the music through the vibration sense
of her hands.
Multimodal plasticity
The capacity to use sensation of the hand as substitution
for another missing sense is a well-known phenomenon which
recently have gained much interest in the neuroscientific
literature (Bavelier and Neville, 2002). Sensory deprivation of
one modality can have striking effects on the development of
the remaining modalities, and it is believed that specific brain
areas called polymodal association centres are susceptible to
such cross-model re-organisation (Bavelier and Neville, 2002).
The phenomenon illustrates the capacity of the brain cortex for
rapid synaptic re-organisation when there is a need for such
plastic changes.
Touch, vision, taste, smell and hearing may co-operate
and interact to give a total appreciation of the environment, but
touch has been recognised as the sense which enables an
ultimate feeling of the true nature of the surrounding physical
world: “touch – the vital medium for appreciation of the
physiological world: we are participants, not spectators, and
it is through embodiment that we participate” (Josipovici,
1996).
Physiology of sensation
The physiological basis for the sense of touch is located in
the fingertips, but the true perception and interpretation is
based on processes located in the brain. The mechanoreceptors
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Lundborg G
of the hand respond to touch, vibration and stretching. They
may be slowly adapting or fast adapting (Edin and Johansson,
1995; Johansson and Vallbo, 1983; Johansson and Westling,
1984; Vallbo and Johansson, 1984). Signals, elicited by tactile
stimuli, are transmitted via nerve fibres of various sizes to the
somatosensory cortical area via relay stations in the dorsal horn
of the spinal cord and at thalamus level. There is a capacity for
plastic synaptic changes between nerve cells at all levels.
According to classic concepts tactile stimuli from the hand are
processed in area 3B in the somatosensory cortex. In the
classical homunculus figures the hand, like the adjacent face
representation, occupies a very large area (Penfield and Boldrey,
1937; Penfield and Rasmussen, 1950) – a fact reflecting the
enormous quantity of nerve cells which are required to serve all
the fine sensory functions of the hand (Kaas, 1983; Kaas, 1997).
Modern brain imaging techniques like PET, MEG and fMRI have
created new and improved possibilities to map the projectional
sites of the hand and fingers, verifying what has been known
from previous studies using direct recordings from a cortical
surface in primates (Merzenich and Jenkins, 1993; Merzenich
et al., 1978; Merzenich et al., 1983). Sensory messages from
the hand are processed mainly in the contralateral hemisphere
but also to some extent in the ipsilateral hemisphere (Hansson
and Brismar, 1999). The large hand projectional area in the
somatosensory area is reflected in an analogous large area in
the motor cortex, reflecting the need for sufficient brain capacity
to control the fine movements of the hand. Also motor functions
of hand are based primarily on activity in the contralateral
hemisphere, but with more delicate hand movements more
areas are being engaged in numerous parts of the brain, including
the ipsilateral side (Ehrsson et al., 2001). It has recently been
shown that electrical microstimulation of motor cortex in
monkeys may not only result in activity in separate muscles or
muscle groups, but may also -when performed on a behaviourally
relevant time scale- evoke coordinated complex movement pattern
of the arm that involve many joints. For example, stimulation of
one site cause the hand to shape into a grip posture and move
to the mouth (Graziano et al., 2002).
Changes in functional organisation
of brain cortex
It was long believed that the synaptic networks and
functional organisation of the brain were hard wired from birth
and could not change during adult life. However, about 20 years
ago experiments involving direct cortical recording from brain
cortex in monkeys clearly shown that the cortical functional
synaptic organisation can rapidly be changed as a result from,
e.g. de-afferentiation and increased use of the hand (see review
by Lundborg, 2000). The hand can shape the brain -from the
functional point of view- during various types of learning processes.
It was early shown in primate experiments that increased use
of fingers gave rise to a rapid functional re-organisation in
somatosensory brain cortex expressed in an expansion of the
projectional sites of the corresponding fingers (Jenkins et al.,
1990; Merzenich and Jenkins, 1993). More nerve cells became
engaged in specific tasks to make possible a more refined
processing of the sensory message from the hand. The same
phenomenon has been noticed in blind patients using their index
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fingers for reading in Braille (Pasqual-Leone and Torres, 1993).
Among musicians it has been demonstrated that the string hand
of violin players, especially those how started practicing in very
early ages, occupies larger projectional area in the somatosensory
as well as motor cortex of the brain (Elbert et al., 1995). Long-
lasting intense activities in the synaptic interactions between
nerve cells induce a strengthening of their connections to adjacent
nerve cells by potentiation of the synaptic sites, hereby increasing
the total cortical area being involved in the tasks. It can be
shown experimentally that the “microspikes”, representing the
synaptic interactions between nerve cells, are becoming more
numerous and more well expressed in these situations, a
phenomenon which reflects the cellular basis for a learning
situation. A number of stimulatory factors such as an enriched
environment can very substantially influence the activation of
such microspikes and hereby facilitate a learning process
(Johansson, 2000).
Brain plasticity
Enlargement of the cortical projection of the hand, based
on increased use of the hand, is an expression for brain plasticity
- the capacity for the brain to “mould its functional shape”
depending on peripheral requirements. The phenomenon is the
basis also for modern trends in rehabilitation of stroke patients,
using so called constrained-induced (CI) training of paralytic
patients to improve motor activation, probably by enrolling new
cortical brain areas in the motor tasks which are required (Candia
et al., 1999; Johansson, 2000; Taub et al., 2002).
Thus, the well-defined cortical hand map can be modified
and enlarged by increased use of the hand, but it can also be
modified in a negative direction by non-physiological use of the
hand. In fact the phenomenon of dystonia which is sometime
seen among musicians, has been explained by a deterioration of
the hand map into a disorganised pattern (Bara-Jimanez et al.,
1998; Byl et al., 1996; Elbert et al., 1998). Dystonia is an
incapacity to regulate and control individual finger movements -
an expression for non-syncronus muscle movements. It has been
shown in primate experiments, where monkeys have been trained
to use their hands in a monotonous, repetitive non-physiological
movements involving simultaneous tactile stimuli of various part
of the hand, that there is a “fusion” of the normally well separated
projectional sites of individual fingers, and that the cortical hand
map hereby is deteriorated (Wang et al., 1995). An analogous
phenomenon has been observed in guitar players suffering from
dystonia (Elbert et al., 1998). Current rehabilitation programs
for these patients aim at a reversal of these pathological
organisational changes towards a normalisation of the sensory
hand map, in order to provide conditions for better coordination
between the sensory and motor components of the central
nervous system (Byl and McKenzie, 2000).
Cortical functional re-organisations can occur as very rapid
phenomena. It has been shown that when fingers are
anaesthetised by local blocks there is, within minutes, a cortical
expansion of the adjacent fingers representation so that their
occupational areas now will cover the former projectional site
of the anaesthetic finger (Rossini et al., 1994).
A strange phenomenon, probably illustrating a bilateral
cortical reorganisation as a consequence of unilateral de-

afferentiation has recently been described by Werhahn (Werhahn
et al., 2002). This author assessed the tactile spatial resolution
of one hand by using Tactile Acuity Gratings (MedCore,
www.med-core.com) in a grating orientation task (GOT). They
found a rapid improvement in tactile spatial acuity and changes
in cortical processing for the left hand during cutaneous
anaesthesia of the right hand. They concluded that this site-
specific improvement in tactile spatial acuity may represent a
behavioural compensatory gain.
A rapid cortical re-organisation occurs also after
amputation of fingers(Merzenich and Jenkins, 1993; Merzenich
et al., 1984; Weiss et al., 2000). Data from brain imaging
studies clear demonstrate how the projectional sites of remaining
fingers rapidly expand - a phenomenon which is even more
obvious after amputation of hands or total arms. After arm
amputation there is a rapid expansion of the adjacent cortical
face representation which expands over the former arm
projection. This may give rise to a very strange phenomenon
already at 24 hours after amputation: the missing hand can be
“mapped” in the face so that touch of specific areas of the face
can give rise to tactile sensations in individual fingers of the
missing hand (Borsook et al., 1998; Flor et al., 1998; Flor et
al., 1995; Ramachandran et al., 1992). The phenomenon of
phantom sensations is based on such, sometimes very disturbing
cortical reorganisation phenomena. It is believed that the more
severe cortical re-organisation, the greater is the risk to develop
pain in association with phantom sensations (Birbaumer et al.,
1997; Flor et al., 1998; Flor et al., 1995; Knecht et al., 1998a;
Knecht et al., 1995; Knecht et al., 1998b). The cortical re-
organisation which follows amputation of a hand can reversed
when the amputated body part is re-attached. In homologous
hand transplantation it has been demonstrated, using fMRI
techniques, that transplantation of a homologous hand to a
amputee is followed by a continuous expansion of a corresponding
projectional hand area in motor cortex. After transplantation
movements are initiated very early in the transplanted hand.
This puts special demands on the motor cortex where an
increasing population of motor nerve cells become engaged in
these movements. As a result, the hand motor projectional
area is regained within six months (Giraux et al., 2001).
Nerve injury
It is well known from primate experiments that transection
and repair of major peripheral nerve trunk is followed by major
functional cortical re-organisations (Garraghty et al., 1994;
Merzenich and Jenkins, 1993; Silva et al., 1996; Wall et al.,
1986). These phenomenons are reflected in the inferior results
usually obtained in patients with injury to major nerve trunk in
the hand or arm. Major nerve lesions in adults represent one of
the most challenging problems to the hand surgeon (Lundborg,
1988). Following repair of the median nerve in an adult patient
there is never, or very seldom a total recovery of the functional
sensibility of the hand. For instance, two point discrimination
very seldom reach normal values and the patients have substantial
difficulties to identify textures and shapes by fingertip sensation
without using vision as a supplementary sense. A major reason
is the misdirection of the outgrowing axons, regardless of how
refined surgical technique is used, so that non-correct skin areas
The hand and the brain
of the fingers are being reinnervated. The result is a total re-
organisation of the cortical hand map – “the hand speaks a
new language to the brain”. The mind of an adult patient has
difficulties in interpreting the new sensory messages, arriving in
new and in-appropriate cortical destinations, and the tactile
gnosis therefore does not return easily. In very young patients
the situation is different: up to the age of 10 there is a possibility
for total recovery of all delicate sensory functions, but then
there is a rapid decline in this capacity to the age of 20-25
(Lundborg and Rosen, 2001). The young brain makes however
a much better job then the adult brain – in analogy with other
types of re-learning processes. In fact, the pattern of sensory
recovery as related to age is analogous to the capacity of
immigrants of different ages to learn to speak a second language
(Johnson and Newport, 1989; Barinaga, 2000). Thus, the key
to the outcome from nerve repair is – to a large extent – hidden
in the brain, and future strategies to improve the results should
be more directed to the process of re-learning rather then the
technical aspects of the surgical repair perse.
Although the necessity of programs for sensory re-
education have been well recognised by e.g. Dellon ( Dellon,
1981;Dellon, 1997), Wynn-Parry (Wynn-Parry and Salter,
1976), these programs for sensory re-training are initiated at
first at the time when the first re-generating fibres arrive in
the hand, i.e. at 3-4 months after repair of a median nerve
injury at wrist level. Immediately after nerve transection there
is a “black hole” in somatosensory cortex – a vacant area
receiving no sensory impulses. The adjacent cortical areas
rapidly expands and take over the former hand area as a result
of a functional re-organisation. At a later stage, when
misdirected axons are re-innervating the hand, there is a second
phase of re-organisation with remapping of the cortical hand
area as a result of nerve fibres arriving in non-correct
destinations in the hand (Merzenich et al., 1983; Wall et al.,
1986).
Artificial sensibility
Thus, a key problem is the first postoperative months when
the hand is without sensibility and the cortical hand representation
is more or less absent. We have started to use a new protocol
aiming at a preservation of the original hand map by using an
alternate sensory input from the hand by use of a system providing
artificial sensibility. From the first postoperative day after nerve
injury our patients use a Sensory Glove system where miniature
microphones are mounted at fingertip levels -either individually
or in a glove- picking up the friction sound which is elicited
when the hand touches various materials, textures and structures.
This friction sound is very specific for individual textures and
materials. By using a stereo system equipped with headphones
there is a stereophonic acoustic spatial resolution of the hand
- “the patient can listen to what the hand feels” (Lundborg et
al., 1999). The result is an immediate capacity to identify various
materials and structures which are touched, and a capacity to
localize and identify individual fingers during touch. The protocol
is used to preserve the cortical hand map and thereby facilitate
sensory recovery when nerve fibres arrive in the hand. Preliminary
results from a Swedish multi centre study and pilot cases indicate
that return of tactile gnosis after six months is significantly
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Lundborg G
improved in patients using the sensory glove system early
postoperatively as compared to control groups (Rosén and
Lundborg, 2002).
Enhanced sensory re-learning (ESR)
In our new protocols for enhanced sensory re-learning (ESR)
the early application of artificial sensibility by using the Sensor
Glove System is an important component to substitute for lacking
sensory input in the first phase after nerve injury. However, also
in the later phase, with beginning re-innervation of the hand
we feel that current programs for sensory re-education can be
much improved based on modern trends in neuroscience
(Lundborg, 2002; Rosén, 2003) The multimodal plasticity of
the brain (Bavelier and Neville, 2002) should be better utilised,
not only expressed in use of artificial sensibility (by the Sensor
Glove System) in the early phase, but also in a way where all
senses are involved in the later training phase when the re-
innervation of the hand has started. Touch, vision, smell, taste
and hearing should all be used together in order to facilitate
return of function and sensibility. An example is given by training
protocols which include tactile meals where e.g. peeling of an
orange, feeling shrimps, sorting and eating candies and crispy
chips of various shapes and sizes can be involved. These activities
involve simultaneous sensation, hearing, vision, smell and taste.
In the training program both hands should be simultaneously
involved since contralateral as well as ipsilateral pathways to
brain cortex hereby can be utilised: the healthy hand is coding
for the injured hand.
Conclusion
The brain controls the hand, but we should also be aware
of that the hand shapes the brain in functional terms. Increased,
decreased or non-physiological use of our hands as well as various
injuries involving de-afferentiation or misdirection of regenerating
axons after nerve repair is followed by substantial re-
organisational phenomena in brain cortex. Whatever happens
to the hand is reflected in re-organisational changes in brain
cortex. In this perspective it is important for hand surgeons to
widen their perspectives from the periphery to include also the
central nervous system. The hand has been regarded as an
extension of the brain to the environment. However, may be we
should rather regard the brain as an extension of the hand into
our mind exploring and revealing the secrets of the surrounding
world.
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