A functional neurodynamics for the own body - II

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4. Reorganisations of the functional structure following a deafferentation

The existence of a permanent potential for functional reorganisation has been

demonstrated at the beginning of the 80s by the research on hand representation

in the monkey’s somatosensory cortex (3b) undertaken byMerzenich and

his lab (Merzenich et al. 1984; Wall et al. 1986). The consequences of more or

less important deafferentations, such as the amputation of one or two fingers,

severance of the median nerve innervating the skin of the radial half of the palm

and the internal face of the first, second and third finger, localised crushing of

the same nerve, etc., have been controlled by detailed cartographic readings.

This has happened on the basis of intracerebral recordings practised at different

stages of functional recuperation. These manipulations have proved that the

central representations of the body are not subject to a rigid anatomical determinism,

attributing rigidly the surface of each part of the body to a well defined

cytoarchitectonic area of the brain. In contrast, the representations of the body

are far more the expression of a dynamic activity enabling the organism to react

in an innovative way to changes in the sensory inputs in order to maintain the

integrity of the “body image” (tactile sensitivity, somesthesia, motricity) damaged

by the lesion. This activity is displayed at the centre by “movements” in

the cortical representations: expansion or contraction of the individual representations

of the fingers, displacement of the borders between representations

of different fingers, expression of normally latent representations, withdrawal

fromor reoccupation of deafferented regions. At the periphery, one finds correlated

movements in the cutaneous receptor fields (RF2) of neurons belonging

to the same somatosensory cortex: RF expansion or contraction, the appearance

of multiple RFs for one and the same cell, the acquisition of alternative

RFs. As points of reference, I will rely only on the most significant evidence.

In response to the amputation of the index and/or major finger, the cortical

representations of the adjacent fingers extend into the area where the amputated

fingers were represented, and in such a way as to fill the gaps between

the represented fingers, thus re-establishing a new borderline. To the extent

that this borderline passes between the representations of fingers which are

not adjacent in normal anatomy, its emergence appears as a true creation of

the functional dynamism. Here and there, the same neurons which until then

upheld the representation of the amputated finger are reassigned to the re-

presentation of one or the other (but not both of) remaining neighbouring fingers.

Since the expansion of the cortical representations (increase in magnification3)

is coupled with a contraction of the cutaneous receptor fields localised on the

same fingers, the intervening reorganisation results in a refinement of the

representation of the skin, which can be interpreted as an attempt to compensate

for the sensory loss due to the amputation (Merzenich et al. 1984). In response

to the severance and suture of the median nerve (an operation favouring a

reinnervation of deinnervated skin) the neurons dealing with the cortical representation

of the hand begin by losing their receptor fields, which are normally

situated on the internal surface of the fingers 1 to 3, and acquire alternative RFs

situated on the back of these same fingers. Later on, the regeneration of themedian

nerve does not result in a centrally diffuse and random reactivation but

in a reorganisation of the functional representations, which includes persistent

anomalies: discontinuities, delocalisations and superimpositions alongside topographically

localised aspects (Wall et al. 1986). After a transitory transfer

of the RFs of the dorsal surface of the fingers onto their ventral surface, deafferentation

resulting fromthe localised crushing of the median nerve turns out

to be compatible with the reestablishment of correct correspondences between

skin and cortex in the context of a normal topographic organisation of the

somatosensory cortex (Wall et al. 1983).

The cerebral cartography of the monkey has taken advantage of the accessibility

of the somatosensory cortex of the hand in the species under investigation,

namely the owlmonkey, whose brain has no central sulcus. Consequently,

a methodology has been developed making possible the drawing up of veritable

maps of the functional topography of the cortical areas, assigning to these

areas quite specific borders and allowing by means of objective measuring the

demonstration of the occurrence of displacements of these borders. This has

been made possible by the chronic implantation of a grid made of many hundreds

of microelectrodes, combined with the tactile exploration of the hand

by means of a tapered probe designed to make indentations of the skin at the

limit of the visible. In that way, minimal RFs for the neurons under examination

are defined. In the case of humans, the neurophysiological description

of phenomena of functional plasticity, exception made of preoperative and

direct explorations, has depended upon the development of techniques of noninvasive

functional imagery like PET, fMRI, magneto-encephalography (MEG)

and transcranial magnetic stimulation (TMS). Only that these methods can

only offer images of more or less diffuse centres of activation, or else curves of

motor potentials evoked in the muscles through TMS. Thus, even though the

language of “maps” has been retained, the maps in question are very far from

delineating the frontiers of the representations with a millimetric precision approximating

that achieved with animal experiments. As a result, an evaluation

of the amplitude of the reorganisation induced in humans by deafferentations

inevitably has a qualitative character and this whether they are provoked by a

local anaesthetic or are of accidental or pathological origin.4

 

5. Remodelling induced by Experience (1): The somatosensory cortex

Does this reorganisation of the functional architecture induced by deafferentation

(experimental or accidental) depend upon mechanisms essentially different

from those of a remodelling linked to a normal use of the perceptive or

motor organs? The question remains controversial.Whatever the outcome, the

study of deafferentation has brought to light a principle of plasticity pertaining

to the organisational schemata of functional somatotopy. This principle integrates

the neurophysiological correlates of the experience of the body with the

general dynamism of the functional organisation of the central nervous system.

In fact this principle of plasticity is not limited to somato-aesthesia that

interests us in connection with the theme of the body image but also concerns

exteroceptive sensory modalities, in particular the primary visual and auditory

areas (to say nothing of the other senses). Visual and auditory experience

are not rigidly predetermined by the anatomical structure of the receptive surfaces

and the cortical regions. In spite of the textbooks, it is admitted that the

retinotopy of V1 is not the isomorphic (nor deformed) projection of the retina,

the tonotopy of A1 is not the isomorphic projection of the cochlea; rather, the

projective geometry implemented here and there by the brain has to be incomparablymore

complex and dynamic. The way in which this happens should be

such that the bodily experience draws its significance from the autonomous activity

of the organism, which in its effort at a permanently renewed adaptation

to the flux of ever renewed experience, finds in itself the resources needed for

the emergence, the remodelling, and the persistent renewal of its organisational

patterns. This dynamism might eventually prove easier to verify with reference

to deafferentations, which are all the more dramatic because the survival of the

individual depends upon them. But it ought also to be possible to verify the

dynamism in question in the normal circumstances of everyday life. The eminently

plastic usage (depending in part if not entirely on a learning process)

such as the normal use of the skin as an organ of tactile and somesthetic sensitivity,

of the hands as tactilo-kinesthetic organs of action, cannot but bring

with it a reorganisation, or at least a modulation, of functional representations.

These changes, in turn, condition the improvement (or deterioration)

of the behavioural performances.

The cartography of the parietal regions bearing the representation of the

hand in the normal adult monkey is highly variable as regards the detailed

representation of the hands in individual cases, a fact that has convinced researchers

that the maps could not be predetermined with precision by the genes

for all the individuals of one and the same species, nor even onto-genetically

fixed at a precocious stage of development. In contrast, they have to be formed

by the particular use made of the hands by each animal in the course of its

individual history. Here are some of the differences from one individual to another:

the global form of the area responsible for representing the hand, the

total surface of this representation, the magnification of the representation of

the regions of the skin, the surface of the representations of the different fingers,

the disposition of the representations of the dorsal surface of the fingers,

in islets or at the lateral and medial margins, the topological boundaries between

representations – continuity, discontinuity, interpolation, proximity of

the boundaries (Merzenich et al. 1987). Training to detect a difference between

an initial vibratory stimulus applied to a finger and a stimulus of a higher frequency

in a series of stimuli of variable frequency produces a topographical

complication of the representation of the hand, including an extension of the

skin zone stimulated and a shattering of the representation of the stimulated

phalanx. This representational change is correlated with the animal’s progress

in the realisation of the task, that is, in a reduction of its tactile threshold of

detection of the vibratory frequencies, a reflection of the localised improvement

in perceptual discrimination of the skin. All the same, and contrary to

what one might have expected on the basis of the rule of inverse proportionality

between the extension of cortical representations and the extension of the

cutaneous receptor fields, this representational change does not correspond to

a shrinking of these receptor fields. On the contrary, one notes an extension, a

multiplication and amutual overlapping of RFs of the neurons dealing with the

representations of the hand subject to training, numerous RFs being displaced

in order to be re-centred and superimposed upon the zone of the stimulated

skin. This reorganisation does not take place on the occasion of a passive stimulation

of the finger, but only when the stimulation is a part of the task, which

suggests that it is under the control of attention (Recanzone et al. 1992).5

In humans, the representational plasticity of the somatosensory cortex

induced by practise has been confirmed for the more complex tasks of professional

life before being confirmed again by artificial tasks controlled in the

laboratory.

Violinists and other players of string instruments continually make use of

the second to fifth fingers of the left hand to press the strings onto the fingerboard

while the thumb of the same hand holds the shaft of the instrument with

frequent changes of position and variations in the pressure exerted. Since the

aim is to ensure a very rapid identification of the right notes with the tips of

the fingers along the entire length of the four strings from the fingerboard to

the bridge, this movement becomes automatic with practise in all gifted musicians.

On the other hand, the movement of the right hand which holds the

bow between the thumb and the index (and middle) finger, by blocking (albeit

with great flexibility) the individual movements of the fingers is less muscular

and constantly calls for the sort of considered decisions in which the artistic

personality of the musician is expressed. A practise of this kind normally initiated

at an early age and continued throughout an entire life-time for several

hours a week brings with it a considerable disequilibrium in the sensory input

of the two hemispheres of the brain. Researchers are interested in the remodelling

of the cortical maps of the hand induced by this intensive and highly

differentiated use of the fingers.

A tactile stimulation from a (painless) pressure applied with a pneumatic

stimulator either sometimes on the thumb and at other times on the little finger

of each hand evokes cortical responses which can be recorded on MEG.

The representative vectors of the equivalent current dipoles which summate

the contributions of the flows of dendrite currents registered in different subjects

are transferred on an fMRI image of the cortex of a control subject. It is

observed that these vectors, which represent the localisation and the average

intensity of the foci of cortical activity corresponding to the individual stimulation

of the thumb or little finger are extended and displaced towards the

median plane with musicians, and this all he more so when the practise of the

instrument begins at an earlier age. The authors infer from this that the size of

the cortical representations is not genetically determined but rather modified

by practise, and that the expansion of the representation of the fingers of the

left hand induced by learning the string instrument can afford the musician a

decisive advantage in responding to the demands of this art, to the extent that

this expansion reflects the enlistment of a more extensive neuronal network for

the processing of a larger flux of tactile information with the musician than the

non-musician (Elbert et al. 1995). The focal dystonia of musicians,6 which can

be correlated with a fusion (without topographic disorganisation) of the representations

of the different fingers on the map of the affected hand, proves that

this remodelling by practise can be converted into a handicap when this usage

is overdone and a lesion is brought about in the central sensorimotor system

by the synchronically abnormal, repetitive and prolonged movements of the

hands (Elbert et al. 1998).7

In a recent experiment, subjects had to recognise as quickly as possible

the orientation of tactile stimuli consisting of three little pins arranged in an

arrow pointed at random towards the right or left, and this by pressing a button

with the right hand. These stimuli were applied simultaneously on the last

phalanx of the thumb and the little finger of the left hand for 50 msecs in a

massive and repetitive way for 1 hour a day over 4 weeks. A high resolution

electro-encephalogram shows that the passive tactile stimulation of a finger

elicits on the scalp an electric field at a latency of 50 to 60 msecs and that the

source of this field can be modelled with an electric dipole situated at the level

of the somatosensory cortex. An electroencephalogram recorded at the beginning

and at the end of the period of training makes it possible to establish, by

projecting it on a MRI image of the brain of each subject, the occurrence of

any displacement of the localisation of the source of the electric field induced

by a new stimulation of the trained thumb and little finger.With regard to the

localisation of the cortical representations of these fingers, it appears that their

simultaneous stimulation in the context of the task of discrimination produces

an effect contrary to their individual and passive stimulation. The representations

of the thumb and the little finger of the right hemisphere (contralateral

to the trained hand) move away from each other in the medio-lateral axis as a

result of the training, denoting an expansion of the areas of representation and

from there a disassociation of those neuronal groups activated by each representation.

When, on the contrary, the stimulation is applied separately to the

two fingers with a random orientation of the stimuli which the subject does not

have to identify, the representations of the thumb and little finger get closer to

each the other, to the point of superimposition, translating an overlapping of

the areas of representation under the effect of a passive stimulation. In their interpretation,

the authors do not decide between two hypotheses: (1) a unique

map of the hand whose activation is differentiated as a function of the different

ways in which the stimulus is processed; (2) multiple maps coexisting in

the same cortical area and whose activation is a function of the context (Braun

et al. 2000).

 

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