jeudi 25 juin 2009

Borje Cronholm: a pioneer in the modern study of phantom limbs

Phantom limbs are endlessly fascinating. I will post regularly about this phenomenon in this blog, for there is so much more to learn about phantoms than is generally realized. Phantom limbs certainly are the first building blocks for a serious phantomology - a science of human bodily consciousness - to emerge. Not only there is much much more to learn, but most of what we do know was actually discovered long ago.

You might have heard of so-called referred sensations in amputees. This refers to the peculiar experience some amuptees have to feel their non-existent limb when certain parts of their bodies are touched. The excellent VS Ramachandran is usually credited with this beautiful observation, which he showed to behave in a strikingly ordered somatotopic fashion (see the now classic review here). It turns out you can literally draw a hand on the ipsilateral cheek an upper limb amputee, delineating as it where the receptive fields that have been rearranged in the somatosensory cortex. Well, that was a brillant rediscovery and extention of an old observation.

I don't know for sure who wrote first about referred sensations in amputees, but the best treatment to have been given to the topic has certainly been published in 1951.
Cronholm B. Phantom limbs in amputees: a study of changes in the integration of centripetal impulses with special reference to referred sensations. Acta Psychiatr Neurol Scand Suppl 1951; 72: 1–310
(A review of this remarkable monography can be found here (The Journal of Bone and Joint Surgery 1953; 35-B (2): 332))

Some information about the author of this work, Börje Cronholm, can be found on the swedish Wikipedia [1]. He was born on 1913 August 28 in Lund and died in Stockholm in 1983, October 11, from a brain tumour. Cronholm spent much of his professional career as a psychiatrist and professor of psychiatry at the Karolinska Institute. He did his PhD on phantom experiences in amputees, which I guess is the work contained in the superb monograph I'm about to present. Cronholm had 3 children, one of which (Tomas) became also became a professor at Karolinska. One of his grand-daughter is apparently a famous artist in Sweden (Ellén Cronholm). Apart from his work on phantom limbs, Cronholm was very interested in the links between art and medicine. He wrote on the artistic expressions of schizophrenic patients (among them one Ester Hennings, whom he met during a temprary position he held at Beckomberga, the mental Institute in Stockholm. Cronholm contributed to the saving of Henning's works, which are now kept and visible at the National Museum). In his later years, Cronholm focused on "psychological measuring methods", meaning he devised clinical tests for assessing memory disorders, the effects of brain damage and aging, as well as depression (I don't know any of these works). He was of course member of numerous boards and associations (which is something I'm afraid I'll never be able to brag about). Intriguingly, it seems that Cronholm was appointed to hold the speech for the Nobel Prize acceptance of Konrad Lorenz. I might investigate a little bit on this, I don't see the connection between these two guys. Well, that's pretty much it for his biography. Let's look now at what I take to be his magnum opus, of which I proudly own one copy. See the cover below, and I ask you to take a good look at the dedication in the upper right corner (see the magnification right below):

I guess to most people this doesn't mean much, but it turns out that the copy I own belonged to JM Nielsen, a neurologist in Los Angeles that produced quite a few inspiring and important papers on disorders of the body schema, back in the 1930's. For example this one, from 1937 in the obscure Bulletin of the los Angeles Neurological Society (and long before people started using the horrible and misleading word "asomatognosia"):

It seems to me that Nielsen deserves to be rediscovered (see some publications here). He wrote numerous papers on a wide range of subjects, and also the influential textbook: Nielsen, JM, Agnosia, Apraxia, Aphasia. 2nd Ed. New York: Hoeber, 1946; as well as A Textbook of Clinical Neurology
. New York: Hoeber, 1941. Here's what Joe Bogen, the famous surgeon of the split-brains, had to say about Nielsen:
I remember one of his brain cuttings relevant to this paper: After someone had read the history, he said, "Let's look at the anterior commissure." He held the brain with one hand and that big knife in the other (as you know, the anterior commissure is shaped like a handlebar mustache) and he made one curving sweep through the brain; then he lifted off the top half, and there was the full extent of the commissure.
Not impressed? Bah, you've never been to a brain cutting demonstration. Anyway, enough of memorabilia, and let's examine some of the book's content. First, as the title indicate, the book is really focused on the phenomenon of referred sensations. It is quite extraordinary that Cronholm devoted such a meticulous work to a phenomenon that, when you think about it, does not immediately strike you as even remotely interesting. Amputees must have noticed for centuries that when certain parts of their body are touched, they "feel" another touch in the location of the phantom limb. Ramachandran ended up with the sexy "remapping" explanation, in the light of the mid-eighties mounting evidence for massive cortical plasticity in the monkey's somatosensory cortex (Kaas, Pons, Merzenich [2]), but before that it took Cronholm to investigate systematically, and I mean really systematically, how these sensations work. He painstakingly interviewed 122 amputees and did all sorts of tests, mostly on tactile perception, with them. The monograph is replete with fantastic illustrations and numerous tables. The table of contents itself tells a whole story (chapter 13: Voluntary movements in a Ph[antom]; chap. 28: changes in the length of a Ph[antom] on stimulation of the stump; chap. 34: Referred sensations assigned to a Ph[antom] or the stump percept when the bladder is expanded, on miction or defecation; chap. 39: The experience of leg amputees when walking with a prothese; etc.)

So below is an illustration of referred sensations in one patient, clearly showing that face-to-phantom referrals where abundantly described before Ramachandran. This is patient n°13, a male born1906, amputated from the right upper limb in 1944 and first examined in 1945. I'm telling you, this is a meticulous study. In 1944, n°13 got "his right arm caught in a conveyor belt and torn off just below the shoulder. The nerves were torn off at the plexus". Shit happens. "Ever since amputation the patient had experienced the entire lost limb percept from within, the Ph-hand most clearly, the the Ph-elbow. The Ph-arm was of normal length and volume. it usually hung down his right side with the elbow slightly flexed and the fingers flexed. He demonstrated this posture with his left arm in exactly the same way at examinations in 1945 and 1949." Note how Cronholm is a smart little guy. One of the only ways to test for the "reality" of phantom limbs is indeed to check its consistency across trials. He continues: "The Ph-arm was experienced as "less real" than the left arm percept - "no life in it" - but just as solid. The patient could not make any voluntary movements in the Ph. Attempts to move the Ph-fingers merely led to increased "tingling" and sometimes to a mild feeling of cramp in the Ph-hand. The Ph-arm always felt numb, he had an "icy" feeling in it and a "tingling", "like when one hits one's funny bone, but not so strong". Well, it goes on and on like this. The level of detail is astonishing. (nowadays you can read papers describing fMRI studies of amputees, including having received a human limb graft, with no mention whatsoever of the mere presence or not of a phantom).
Let's look at the figure for patient n°13.

Black dots in (A) indicate the location where the experimenter touches the patient. Each trial is numbered, and the resulting tactile feeling in the phantom arm is shown in (B). Note how touches on the chest elicit feelings in the phantom forearm (with quite large receptive fields), and touches on the stump elicit feelings in the fingers, or rather across several fingers. Note also that here Cronholm didn't check for the face, this will come in the next figure. Cronholm had almost all the cards in his hands to make a point about the somatotopy of these referred sensations and how they could relate to the somatosensory homunculus. The only problem, of course, is that Penfield's homunculus wasn't fully described at the time, or at any rate Cronholm didn't have the required mental framework to draw the connection with the information on somatotopy available in his time (Penfield published with Rasmussen The Cerebral Cortex of Man in 1950, while Cronholm was busy pin-pricking his patients during the 1940's). In any case, it boggles the mind to see that it took 40 more years for Ramachandran to come up with the simple and elegant explanation of cortical maps invading the brain areas left deprived by the peripheral amputation. Well, that's a nice story, as always with Ramachandran, but it turns out that reality is often less spectacular than the textbooks. Cronholm followed-up on patient n°13, and here's in (C) what he obtains 3 years later:

Numbers refer to the same loci of stimulation than 3 years earlier, from the previous figure (Cronholm was a well organized man). Referred sensations from the cheek ipsilateral to amputation elicited wide areas of sensations in the forearm and the wrist. This is rather unlike the classic "hand on the face" of Ramachandran. See also that touches on the chest, this time do elicit sensations in the fingers, whereas touches in the stump produce feelings in the forearm! What the hell? This is the exact reverse pattern from 3 years ago! How does one account for that in terms of cortical remapping? You see, phantom limbs are much more complicated and fascinating than many people acknowledge, including people well versed into neurology and bodily consciousness.

And there are even more bizarre things. Look at the following figure, which shows the phantom forearm of patient n°6, amputated at the elbow in the right arm (this male patient was amputated when he was 7 years old and examined at 17). In (A), Cronholm stimulated the ventral side of the stump, in 13 locations drawing a straight line from the inside of the elbow to the apex of the stump. Doing this, the patient indicated on his healthy arm where the feeling was felt in the phantom, and it turns out that the somatotopy is very reliable: all the phantom sensations were isolated tactile sensation drawing a straight line on the ventral side of the phantom forearm. Now, look at (B). Stimulating the dorsal side of the stump elicited feelings in the dorsal side of the phantom. Right away, this seems to indicate that the phantom has some kind of a volume, or spatial existence. But this is not the most interesting with this figure. You have to read the fine print to see what is really intriguing here. Stimulation n°13 in the apex of the stump, in (A), is not represented on the phantom chart. Why? Well, that because, as Cronholm indicates, "when point 13 was stimulated the patient felt a sensation "in space" distal to the Ph-fingertips"). That's right, exosomesthesia! This patient, quite clearly, makes a difference between a phantom limb and empty space. Think about what this means, I just love this observation.

There is much more to say about Cronholm, so stay around for future posts on this classic, but poorly known, research on phantom limbs. What I can say right away, however, is that where Cronholm is excellent in observation, he's rather weak on theory. But reading this painstakingly documented monograph, one gets the impression that he wanted to give the best possible picture, with any single detail that might turn out later to be relevant or not, for others to study.

[1] Thanks to Pär Halje for express translation (with ever so honey-coated voice)
[2] Animal activists out there behold: these guys simply chopped off monkeys fingers and limbs to see what would happen in their brains. Well, they usually made up some story about the animal "losing" "spontaneously" its body parts in some fight, but it's clear that this sort of neuroscience is by now over (or at least I hope so).

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