RamaTochingHandlikePhantom09.pdf

(63 KB) Pobierz

OBSERVATION

Sensations Evoked in Patients With Amputation

From Watching an Individual Whose Corresponding

Intact Limb Is Being Touched

Vilayanur S. Ramachandran, MD, PhD; David Brang, MA

Background:

After amputation of a limb, the majority

Design:

Case report.

Setting:

University campus, academic setting.

Patients:

Four patients with upper-limb amputation.

Main Outcome Measures:

The subjective reports of

of patients experience phantom sensations, such as phan-

tom pain. Such patients provide an opportunity for the

exploration of the perceptual correlates of recently dis-

covered “mirror neurons,” which fire not only when in-

dividuals move their own limb but when they watch the

movements of the corresponding limb of another per-

son. Similar neurons exist in the secondary somatosen-

sory cortex for touch: they fire when the individual is

touched or simply watches another person be touched.

While these neurons cannot by themselves discriminate

between the two, the mind is aware of the difference be-

tween feeling and watching; one does not confuse em-

pathy with actual experience.

Objective:

To investigate whether patients with ampu-

tation experience the sensations of another person in their

own phantom limb during the mere observation of some-

one else being touched, owing to removal of the inhibi-

tion of the mirror neuron system that would have oc-

curred had the limb been intact.

patients.

Results:

We report that 4 individuals with arm ampu-

tation, the mere watching of the intact hand of another

being touched evokes vivid, precisely localized sensa-

tions in their own phantom hands.

Conclusions:

We suggest these evoked sensations are

owing to removal of neural signals from the hand that

would have ordinarily inhibited the response of the mir-

ror neurons and prevented their activity from reaching

the threshold of conscious awareness.

Arch Neurol. 2009;66(10):1281-1284

someone else being touched.

5,6

This raises

an interesting question: how does the neu-

ron know what the stimulus is? Why does

the activity of these neurons not lead one

to literally experience the touch deliv-

ered to another person? How does “one-

self” know who is being touched? One pos-

sibility is that the tactile receptors in the

skin tell the other touch neurons in the

cortex (the nonmirror neurons) that they

are not being touched, and this null sig-

nal prevents touch sensations from reach-

ing the threshold of conscious aware-

ness. The net result is that one empathizes

with but does not actually experience the

touch quale.

This hypothesis, even though it is

speculative, makes a straightforward but

counterintuitive prediction. If one’s arm

is amputated, one should suddenly start

to experience the sensations of the same-

side arm of other people

when one

watches them. We had earlier seen pre-

Author Affiliations:

Center

for Brain and Cognition,

University of California

San Diego, La Jolla.

tal cortex send signals

down the spinal cord that

orchestrate skilled and

semi-skilled move-

ments such as putting food in the mouth,

pulling a lever, pushing a button, etc.

These are “ordinary” motor command neu-

rons, but some of them, known as mirror

neurons, also fire when one merely

watches another person perform a simi-

lar act. It is as if the neuron (or, more

strictly, the network of which the neuron

is part) used the visual input to do a sort

of “virtual reality simulation” of the ac-

tions of the other person. This allows one

to empathize with the other person and

view the world from his or her point of

view.

2-5

There are also “touch mirror neu-

rons” in the secondary somatosensory cor-

tex that fire not only when the skin is

touched but also when one merely watches

EURONS IN THE PREFRON

(REPRINTED) ARCH NEUROL / VOL 66 (NO. 10), OCT 2009

1281

WWW.ARCHNEUROL.COM

Downloaded from

www.archneurol.com

at University of Massachusetts Boston, on May 11, 2012

liminary hints of such a finding and now report the re-

sults of systematic experiments.

METHODS

Four patients (referred to herein as patients 1-4) with upper

limb amputations who reported having experienced vivid

phantom limb sensations were recruited for the experiment.

8-10

One of the patients had been studied previously by V.S.R. and a

colleague.

Patient 1, age 22, had undergone amputation above his left

elbow 11 months previous to testing, following a crushing in-

jury. Patient 2, age 21, had undergone amputation 7.62 cm be-

low the right elbow 12 months previous to testing. His arm had

been severed in an army vehicle accident. Patient 3, age 50, had

undergone amputation above the left elbow following a sar-

coma 4 years previous to our work with him. Patient 4, age 40,

had had a left brachial avulsion 24 years previously and am-

putation 12 years previously. All were mentally lucid. None had

any other neurological abnormalities except for Horner syn-

drome in the left eye of patient 4. None of the patients was aware

of the purpose of our experiments.

We requested that an assistant place her hand on a table in

front of patient 1 so that it was close (eg, 30.48 to 45.72 cm) to

the phantom hand of the patient but not actually on top of it.

The hand of the assistant could either be parallel to the phan-

tom hand or orthogonal to it (at a 90° angle) or pointing in the

opposite direction (ie, toward the patient). We then repeat-

edly stroked and rubbed the hand of the assistant as the pa-

tient watched. Each “stroke” was over a length of 5.08 cm on

the skin of the assistant and was delivered quickly (a one-half

second duration) 10 times with an inter-stroke interval of a half

second (roughly 10 seconds total); we randomly varied the lo-

cation or direction after every couple of strokes (to avoid ha-

bituation, if any). The patient was asked to report whether he

felt anything on any part of his body, including the phantom

limb. If he reported a sensation, he was asked to say (or point

to) where it was felt.

Each cluster of strokes, which lasted 10 seconds total, was

repeated 8 times, again with a movement to randomly chosen

locations on the hand of the student during different trials. The

8 clusters were separated from each other by 20-second inter-

vals so that the entire session lasted roughly 3 minutes. Since

the patients claimed, without prompting (see the “Results” sec-

tion), that sensations were felt vividly by the phantom hand,

the patients were asked explicitly whether they felt anything

in their intact hand. They reported that this never happened.

We then applied the touch stimuli to the brow of the assis-

tant while the patients watched; we asked whether the pa-

tients felt the touch on their brow or their phantom limb. This

stimulus-and-questioning sequence was repeated 6 times per

patient (the stimulus and intertrial durations were identical to

those of the previous experiment and replicated in all subse-

quent experiments). Lastly, we asked the patient to watch the

assistant while we rubbed a piece of ice on her hand. He was

asked if he ever felt the cold (or any sensation) anywhere on

the body, including the phantom limb. This was repeated 6 times

for each patient. The cold trials were done independently, ie,

not interspersed with the touch sessions.

For patients 1, 2, and 3, the experiment was repeated 2 weeks

later by means of identical procedures and an identical num-

ber (8) of trials for each patient. The entire experiment was re-

peated for patient 4, by means of the same experimental pro-

tocol except that the 2 testing sessions were separated by 2

months. For patient 4, special attention was paid to topogra-

phy; ie, to see if the location of referral to sensation depended

on the specific part of the hand of the assistant that was touched

(eg, thumb, index finger, palm, etc). We also repeated the ice

experiment with him.

Finally, 16 control individuals with no amputations were

recruited. The protocol used was similar (but since no referral

was given by any control individual, the procedure was not re-

peated a week later). The instructions given were identical.

RESULTS

Patients 1 through 4 experienced vivid and consistent re-

ferral on almost all trials (61 out of 64). The 3 trials in

which patient 2 experienced hesitation or doubt were

counted as “no referral.”

The subjective accounts of the patients were interest-

ing. All stated they were surprised by the experience, es-

pecially during the first few trials (comments included,

“It’s spooky, sir” and “Well, I learn something new about

my phantom every day”). All of them claimed to expe-

rience a latency of about 5 seconds during the first 3 or

4 trials (and a latency of 1 or 2 seconds on subsequent

trials) before the referral occurred and asked us why this

was the case. Patient 4 commented that this latency may

have been the reason he had not noticed the effect him-

self before this experiment (“Sensations sometimes come

and go, and I probably wasn’t paying attention—nor do

I often continuously watch people stroke themselves in

the manner you just did”).

The topography was also nearly always stable and con-

sistent for patient 4. The stroking of the thumb of the

assistant elicited sensations of being stroked on the phan-

tom thumb, pinky to pinky and palm to palm. The third

and fourth digits were not delineated; on many trials there

was a “diffuse” sensation that spread across and beyond

those digits in the phantom hand when either of those

fingers of the assistant was touched. It was our impres-

sion that there was topography in the other 3 patients as

well, but because they were the first patients to be tested,

we did not have the opportunity to specifically study this

aspect of their referral.

In patients 1 through 3, there was no referral of cold.

They each reported spontaneously that they felt the rub-

bing but not the cold. This was true no matter how long

they watched (“Well, I expect the cold in my phantom,

but I can’t feel it: no wetness, no cold, just the touch”).

This is an important distinction, as it reduces the likeli-

hood that these effects are confabulatory; why would

touch be referred and not cold? Patient 4, however, re-

ported a vivid experience of cold on every single trial:

he seemed amused and surprised by the sensation. He

noted that touch was referred first, followed a few sec-

onds later by the arrival of cold. This was true on all trials.

All 4 patients also noted, 3 without our having ques-

tioned them, that on some occasions when the assistant

wiggled her hand slightly, the phantom limb felt like it

was wiggling. The referral of touch was enhanced, if ini-

tially “primed,” by the wiggle (perhaps by sensory or at-

tentional enhancement of the phantom limb itself). The

reason for this finding is obscure.

No referral was seen for any trial with any patient (to

either his brow or his phantom limb) when the brow of

the assistant was touched. Of the 16 control individu-

als, 15 felt no referral to their own arm(s) on either touch

WWW.ARCHNEUROL.COM

(REPRINTED) ARCH NEUROL / VOL 66 (NO. 10), OCT 2009

1282

Downloaded from

www.archneurol.com

at University of Massachusetts Boston, on May 11, 2012

or cold on any trial. One control individual reported oc-

casional tingling (in 3 out of 8 trials) in the hand but said

the tingling was very feeble.

COMMENT

The results clearly show that when a person who has had

a limb amputated watches the corresponding intact limb

of another person being touched, the former person ex-

periences it in his or her phantom limb. The referral was

organized topographically, especially with Patient 4, al-

though with poor resolution between the third and fourth

digits. The other 3 patients also demonstrated topogra-

phy but were not tested systematically for this purpose.

Stroking along the length of the index finger, however,

produced a sensation of being stroked on the phantom

index finger in all 4 patients.

We interpret these results in terms of the known prop-

erties of the mirror neuron system (MNS), which is ac-

tivated both when one is touched and when one watches

someone being touched. The reason one does not liter-

ally experience touch when someone else is touched is

because, we suggest, the “null” signal from an intact hand

prevents activity in the MNS from reaching the thresh-

old for conscious awareness. The amputation removes

this null signal, thereby causing the patient to literally

feel touch administered to another. It is a sobering thought

that the only barrier that stops one from experiencing

the sensations of someone else is the skin; remove it and

the epistemic barrier between oneself and “other minds”

is also removed.

The lack of referral to cold in patients 1 through 3 is

noteworthy and may reflect the fact that most individu-

als do not have “temperature mirror neurons” or per-

haps have few of them. The manner in which mirror neu-

rons are constructed is unknown but if it is, at least in

part, based on Hebbian associative learning rather than

being hard-wired (“I feel touch whenever I see someone

touch my hand, etc”), then it is possible that these learned

associations are more prominent for touch than cold. These

lifelong associations may depend on previous experience

with ice, which would produce individual differences; this

factor would account for the experience of patient 4.

We considered the possibility that these effects are con-

fabulatory in origin. This is unlikely for 5 reasons. (1)

None of the patients knew (nor were they told) what to

expect. (2) The patients were genuinely surprised and

intrigued by these observations. Patient 1 even added that

after we had demonstrated this, he had gone home and

asked his wife to massage her own hand while he watched,

and watching her do so seemed to relieve his phantom

pain. (3) In patients 1 through 3, there was referral of

touch but not cold. If these patients were confabulating,

why would they each independently report this find-

ing? Each patient reported being surprised by this un-

coupling. (4) In all patients there was a latency of a sec-

ond or two before referral was felt, which would be a

curious thing to confabulate. (5) No referral was ever re-

ported to have been felt in the intact hand.

Additional informal observations deserve mention. We

tried stroking a crushed piece of tissue paper while pa-

tient 4 watched. He responded with a slightly amused

chuckle, “No, I don’t feel the paper texture or anything,

just a diffuse touch.” Tactile “texture-detecting” cells

(probably in the secondary somatosensory cortex) may

not be adequately wired to the MNS; the other 3 sub-

jects had not been tested in an experiment that used

crushed tissue paper. Nor was there any referral of pain

when the assistant was observed being poked with a

needle. This finding, too, argues against confabulation.

patient 4 said he could feel the indentation on the skin

but no pain. For practical reasons, this experiment could

not be carried out with the other patients.

It is important that 15 of 16 control individuals ex-

perienced no referral to their intact hands. It is unclear

why the 16th control individual experienced some vague

“tingling” during 3 trials, but perhaps there is incom-

plete vetoing of the MNS in this individual, which causes

some “leakage” of MNS activity into consciousness (ie,

the distinction between actual sensation and empathy was

muddled). No biological system is perfect. This obser-

vation of “leakage” in control individuals is not unprec-

edented. In what may have been the earliest observation

of the MNS in action, Charles Darwin

commented, “Thus

persons cutting anything with a pair of scissors may be

seen to move their jaws simultaneously with the blades

of the scissors.”

What is new in our present study is the

demonstration that the removal of real sensory input can,

by itself, increase the MNS activation so that it emerges

into consciousness.

The sensations one experiences consciously in daily

life do not depend only (or even mainly) on a direct “hot-

line” from sensory channels to sensory brain areas, but

on interactions within complex multimodal networks,

of which the MNS is an important part. By changing parts

of this network, one can literally feel the sensations of

others. Indeed, it may not be too radical to suggest that

the brain is in a state of dynamic equilibrium not just with

regard to sensory input, but also with other brains, in the

earliest stages of neural processing. Thus, the “privacy”

of qualia, to which philosophers give so much impor-

tance, is an illusion.

An important observation by Blakemore and col-

leagues

is also relevant to this discussion. They ob-

served a new form of synesthesia: an otherwise healthy

individual who experienced touch when simply watch-

ing others being touched. They suggest that this may re-

sult from a congenital hyperconnectivity within the MNS

system itself.

Aside from the theoretical implications, our observa-

tion may also be of clinical interest. Recall that patient 1

observed that if he simply watched his wife massage her

own hand, it seemed to partially relieve his phantom pain.

Obviously, the information is merely anecdotal at this

point but it raises therapeutic possibilities. Similarly, the

efficacy of mirror visual feedback in the treatment of stroke

and phantom pain

10,13

may partially rely on the reactiva-

tion of portions of the MNS that are repressed or ren-

dered dormant as a result of disease. One also wonders

whether even a “real” pain (as in complex regional pain

syndrome) would be reduced if the patient were merely

to watch the corresponding location on the arm of an-

other person be massaged. The time course of the effect

WWW.ARCHNEUROL.COM

(REPRINTED) ARCH NEUROL / VOL 66 (NO. 10), OCT 2009

1283

Downloaded from

www.archneurol.com

at University of Massachusetts Boston, on May 11, 2012

also deserves study and can be investigated by seeing if

referral occurs immediately after a brachial block in-

stead of merely after amputation.

In addition to their inherent theoretical and clinical

interest, these findings also set the stage for future brain

imaging studies in order to, at the very least, obtain pretty

pictures. Would primary somatosensory cortex activity

be seen to correspond to the amputated arm when a pa-

tient merely watches the intact arm of another being

touched?

REFERENCES

1. Mountcastle VB. The parietal system and some higher brain functions.

Cereb Cortex.

1995;5(5):377-390.

2. Rizzolatti G, Fogassi L, Gallese V. Mirrors in the mind.

Sci Am.

2006;295(5):54-61.

3. Cattaneo L, Rizzolatti G. The mirror neuron system.

Arch Neurol.

2009;66(5):557-

560.

4. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor

cortex.

Brain.

1996;119(pt 2):593-609.

5. Iaccoboni M.

Mirroring people.

New York, New York: MacMillan; 2008.

6. Keysers C, Wicker B, Gazzola V, Anton JL, Fogassi L, Gallese V. A touching sight:

SII/PV activation during the observation and experience of touch.

Neuron.

2004;

42(2):335-346.

7. Ramachandran VS, Rogers-Ramachandran D. Sensations referred to a patient’s

phantom arm from another subject’s intact arm: perceptual correlates of mirror

neurons.

Med Hypotheses.

2008;70(6):1233-1234.

8. Mitchell SW. Phantom limbs.

Lippincott’s Magazine of Popular Literature and

Science.

1871;8:563-569.

9. Ramachandran VS, Hirstein W. The perception of phantom limbs: the D.O. Hebb

Lecture.

Brain.

1998;121(pt 9):1603-1630.

10. Ramachandran VS, Rogers-Ramachandran D, Cobb S. Touching the phantom

limb.

Nature.

1995;377(6549):489-490.

11. Darwin CR.

Expression of Emotion in Man and Animals.

London, England: John

Murray Publishers; 1872.

12. Blakemore SJ, Bristow D, Bird G, Frith C, Ward J. Somatosensory activations

during the observation of touch and a case of vision-touch synaesthesia.

Brain.

2005;128(pt 7):1571-1583.

13. Ramachandran VS. Phantom limbs, neglect syndromes, repressed memories,

and Freudian psychology.

Int Rev Neurobiol.

1994;37:291-333.

Accepted for Publication:

May 26, 2009.

Correspondence:

Vilayanur S. Ramachandran, MD, PhD,

UC San Diego, 9500 Gilman Dr 0109, La Jolla, CA 92093-

0109 (vramacha@ucsd.edu).

Financial Disclosure:

None reported.

Funding/Support:

The authors were supported by fund-

ing from Herb Lurie, JD, Brian Belnap, MD, and Dick

Geckler, MD.

Additional Contributions:

We thank Asha Baxter, BA,

for assistance.

Announcement

Visit www.archneurol.com.

As an individual sub-

scriber, you may elect to be contacted when a specific

article is cited. Receive an e-mail alert when the article

you are viewing is cited by any of the journals hosted by

HighWire. You will be asked to enter the volume, issue,

and page number of the article you wish to track. Your

e-mail address will be shared with other journals in this

feature; other journals’ privacy policies may differ from

JAMA & Archives Journals.

You may also sign up to re-

ceive an e-mail alert when articles on particular topics

are published.

(REPRINTED) ARCH NEUROL / VOL 66 (NO. 10), OCT 2009

1284

WWW.ARCHNEUROL.COM

Downloaded from

www.archneurol.com

at University of Massachusetts Boston, on May 11, 2012

Plik z chomika:

deviler666

Inne pliki z tego folderu:

MirrorMovementsfMRIPain2010.pdf (586 KB)
MirrorN_ModelGraspArbib2005.pdf (1032 KB)
MirrorN_PETPMCactrizzolati-arbib97.pdf (136 KB)
MirrorN_PETrizzolati-arbib96.pdf (5103 KB)
MirrorN_rizzolati-arbib.pdf (183 KB)

RamaTochingHandlikePhantom09.pdf

Plik z chomika:

Inne pliki z tego folderu:

Inne foldery tego chomika: