J7oumnal of Neurology, Neurosurgery, and Psychiatry 1 993;56:329-333

oumrnal of

NEUROLOGYNEUROSURGERY& PSYCHIATRY

Editorial

Penfield's homunculus: a note on cerebral cartography

In 1937, Penfield and Boldrey published a paper ofmajor importance.' They described their work on theeffects of stimulation of the cerebral cortex in man, theprocedures being carried out as exploratory manoeuvresto delineate the appropriate area for subsequent surgicalintervention. They confirmed the precise topography ofcortical localisation, and were able to relate stimulationof a discrete part of the brain with motor and sensoryphenomena affecting a particular part of the body. Whilstthese now classical studies confirmed and greatly extend-ed what had been known from earlier observations inawake humans and from experiments in animals, themanner of presentation of their findings was remarkable.It was the first time pictorial means of illustrating corticalrepresentation had been attempted; it was thus an entire-ly new concept, but it was also one which has proved acurious method of illustration and one which gives rise toa number of unforseen problems.

Penfield and Boldrey set out to illustrate "the orderand comparative extent" occupied in the sensorimotorstrip.' To represent the topography of their observations,the authors departed from the rigorous textual descrip-tion of the effects of stimulation of the brain andachieved an extraordinary conceptual leap: an artist, MrsH P Cantlie, was employed to draw a sensory and motorhomunculus-a term discussed below. This firsthomunculus to be created (fig 1) was described as giving"a visual image of the size and the sequence of the corti-cal areas". It was symmetrical in shape and illustratedboth motor and sensory features together; what actuallywas represented, however, was ambiguous and confusing.The authors state that the size of the parts was deter-mined "not so much by the number of responses...but bythe apparent perpendicular extent of representation ofeach part when these responses were multiple for thesame part". What is meant by "perpendicular" is notstated, and it becomes even less clear from the subse-quent comment: "that the large size of the thumb andthe lips indicates the vertical extent of Rolandic cortexdevoted to those parts in individual cases is very large". Itis unclear whether "vertical" is the same as "perpendicu-lar", and whether these terms mean longitudinal over thecortical surface, or deep-since the authors also stimulat-ed deeper layers of the brain after having resected areasfor extirpation of abnormal brain. The referral toresponses which were multiple for the same part is alsodifficult to interpret, since it could imply multiple siteswere effective in eliciting responses, or that only in cer-

tain areas were multiple sites actually stimulated. Whilstthe homunculus appears to relate to length rather thanwidth, the parts illustrated are in fact enlarged in bothdimensions. Also noteworthy is that responses have beentransposed to the same side of the brain for the purposesof representation, and it is not possible from the illustra-tion to distinguish unilateral from bilateral effects of cor-tical stimulation.

Thirteen years later, in their monograph entitled Thecerebral cortex of man, Penfield and Rasmussen madeanother attempt to illustrate cortical representation.2 Thiswas preceded by a diagram of a cross-section of the cere-

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Figure 1 Thefirst homunculus, Penfield and Boldrey, 1937. Reprintedfrom Brain 1937;60:389-443, with permission of The Macmillan PressLtd.

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Figure 2 The motor andsensory homunculus: the firstmap. Penfield andRasmussen, 1950. Reprintedwith permission ofMacmillan PublishingCompany from The cerebralcortex ofman by WilderPenfield and TheodoreRasmussen. Copyright 1950Macmillan PublishingCompany; copyright renewed1978 Theodore Rasmussen.

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bral hemispheres in which were drawn solid bars at theperiphery, the length of the bars giving an indication ofthe relative cortical areas from which the correspondingresponses were elicited. This implies somewhat differentinformation was being illustrated compared with the1937 illustration. A few pages later, overlying the bars issuperimposed the homunculus, which is again "broughtforth" by the same artist, but in a different and evenmore familiar form, draped along the cortical surface andinterhemispheric fissure. In this homunculus, however,the motor and sensory representations have been separat-ed, slightly modified and corrected (fig 2). These draw-ings are so memorable and have been reproduced sooften that it is difficult to appreciate that here, even moreso than with the first homunculus, a new concept in rep-resentation and imagery had been created. Moreover, forthe first time the homunculus can be considered as someform of "map" of human cortical representation, beingmore or less precisely in relation to actual brain areasidentified at surgery. This compares with the firsthomunculus, which was not drawn in relation to thehemispheres at all. It is unclear whether the authorsappreciated the visual significance of the homunculi, butthese figurines created a precedent which has had a majorinfluence on subsequent forms of related graphic illustra-tion.

Degradation of the homunculus subsequently ensued,with the appearance in 1954 of multiple homunculi.Penfield and Jasper now illustrated three sets of homun-culi (fig 3), the first set (motor and sensory) in relation tothe Rolandic fissure, a second apparently purely sensoryhomunculus in the secondary sensory area near theSylvian fissure, and a third homunculus (virtually onlymotor) in the supplementary motor cortex.3 The homun-culi change considerably in this process; for instance thefingers and toes are made to seem important in the sec-ondary sensory figurine, which is crouched, and is tosome extent bilateral, whereas the supplementaryhomunculus is straight and extremely vaguely represent-ed. The precision intended in the earlier homunculi hasbeen almost completely lost; indeed Penfield and Jasperstated that "the exact position of the parts must not beconsidered topographically accurate. They are aids tomemory, no more". And again, "the figurines...have thedefects, and the virtues, of cartoons in that they are inac-curate anatomically...". It suggests that the homunculushas taken over from its authors, and illustration has out-

stripped the scientific evidence available. Indeed, thebilateral leg movements that can be elicited by stimula-tion of medial structures led Bates to denigrate the con-cept of the homunculus thus: "May it not be, in otherwords, that in depicting the 'average' representation themotor homunculus should have two back legs?"4

Homunculi now appeared in other areas of the brain,such as the thalamus, and Penfield and Jasper3 were thefirst to place a homunculus in this subcortical region (fig4). Whilst they stated a precise topographical organisa-tion is present in the somatic relay nuclei of the thala-mus, the homunculus drawn there "makes no pretence to

SECOND > 'Ib A sSENSORY

Figure 3 Mulltiple sets of homunculi. Penfield and Jasper, 1954.Reprintedfrom Epilepsy and the functional anatomy of the human brain,with permission of Churchill Livingstone.

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Figure 4 The homunculus in the thalamus. Penfield and Jasper, 1954.Reprintedfron: Epilepsy and the functional anatomy of the human brain,with pernission of Churchill Livingstone.

detailed accuracy, though the relationships between bodyparts are probably roughly correct, judging from animalexperiments". The homunculus appears now to havedegenerated into a purely artistic device vaguely based on

animal experimental work, without any scientific basis tojustify the human form portrayed. Final relegation tomere amusement must be the riot of homunculi withnumerous images in the thalamic region depicted byHassler et al5 and further annotated by Creutzfeldt.6Whilst recognising the professional medical illustrator'srole as an interpreter,7 any scientific significance of thesedisplays is difficult to discern.An interesting correspondence is referred to between

Penfield and an un-named "distinguished neurologist",the latter pointing out that Hughlings Jackson had sug-

gested the index finger would have a larger representationthan the others; the discussion concludes by Penfieldstating "the purpose of this monograph is to analyse thedata, however imperfect they may be, without preconcep-tion".) With this stated aim, however, it seems curiouslycontradictory to represent meticulous scientific observa-tions by means of an homunculus. As implied by the pre-ceding comments on Penfield and Jasper's multiplehomunculi, even more than in the earlier homunculi,there is uncertainty as to what actually was being repre-sented. Was it the surface area of the cortex, or thelength or depth, or in addition some measure of thethreshold of stimulation that produced motor or sensoryeffects?

Homunculi perhaps represent different things in differ-ent circumstances. The motor homunculus is some formof representation of areas from which involuntary move-ments can be produced by artificial and passive means; isthis the same homunculus that would be derived follow-ing a different form of cortical excitation such as magnet-ic stimulation, or when voluntary movements aregenerated? This contrasts with the sensory homunculus,which in Penfield's observations denotes areas fromwhich subjectively reported sensations in the peripheryare produced by antidromic rather than orthodromicstimulation. The sensations reported were of varioustypes, and included tinglings, numbness, sensations ofmovement, and rarely pain, feelings of thickness, andother sensations.

This is of considerable importance, since thehomunculus as represented by Penfield gives the impres-sion of single motor and sensory maps. From experi-ments using electrical stimulation techniques in monkeys,however, it seems probable that the concept of simplesomatotopic organisation is inadequate.8 For the sensoryhomunculus, Merzenich et aO provide evidence for multi-ple maps representing different functions, and there isevidence in non-human primates that there are as manyas seven or more somatosensory areas, "most of whichappear to constitute complete, orderly representations ofthe body surface or deep body tissues".10 Apart from dif-ferences that might result from different stimulation tech-niques, it may also be maps of cortical potentials evokedperipherally are not identical to maps of perceived sensa-tions induced by direct cortical stimulation. ThusPenfield's homunculus is not only ambiguous in whatexactly it does represent, but also gives an unjustifiedimpression of cortical representation which is both singleand established.

Moreover, not only were Penfield's data obtainedusing comparatively large-diameter stimulating electrodesin patients with brain disease, but different individuals,both normal and those with diseases of the nervous sys-tem, have very different cortical areas from which sensoryand motor phenomena can be elicited. Penfield wasaware not only of this individual variation but also thatthe effects of cortical stimulation could change aftersurgery.' Whilst the immense plasticity of cortical mapsin animals is established (for review, see Wall"), there arealso several examples of plasticity in humans. Confirmingobservations in animals, patients with damage affectingsomatosensory systems show evidence of marked somato-topic reorganisation at thalamic level.'2 At cortical level,plasticity of maps of outputs of the human motor systemhas been demonstrated after amputation, paraplegia andhemispherectomy, and changes in sensorimotor represen-tation have been demonstrated in blind braille readers(for review, see Pascual-Leone et at"). What of thehomunculus in these patients?

Results of cortical stimulation in animals had of coursebeen illustrated before, for instance by superimposingnumbers and then words for the relevant part on draw-ings of the brain.'4 Nevertheless, the first figurine washuman, with Penfield's homunculus the precedent forthe profusion of illustrations of experimental work onanimals. Fundamental studies on cortical localisationusing stimulation and evoked potential techniques, par-ticularly by Bard, Woolsey et al, were illustrated in analo-gous fashion; the simiusculus, the cortical representationof the monkey, soon appeared, as did cortical representa-tion of the rabbit, rat, cat and doubtless other animals(see Woolsey'5). The pig and its large snout representa-tion was another example illustrated in a different formby Adrian.'6 Interesting, since it showed another form of

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physiological process is the figurine placed in the cerebel-lum by Fulton,'7 and which he called a "primunculus"rather than homunculus. It illustrated the approximatedistribution of excitatory and inhibitory foci in the anteri-or cerebellum. All these animal representations are morefigurative than accurate, contrasting with the extremelyaccurate mapping of localised evoked potentials illustrat-ed diagrammatically rather than by means of figurines.'5

Even as a form of straightforward representation, thehomunculus is curious. Just as the head has been the siteof numerous fantastic yet symbolic compositions sinceArcimboldo in the sixteenth century,'8 so with thetwentieth century homunculus there is artistic licenceand embellishment. The border between fact and imagi-nation has been blurred: the homunculus has beenimbued with character, an attribute which many a viewerwill experience, and which is perhaps unique in terms ofscientific illustration. Thus the first homunculus drawn in1937 is described by Penfield and Boldrey as"grotesque".' The later ones are "brought forth", and thedrawings clearly have expressions and a personality. In1937, the face is smiling broadly and is missing half itsteeth; the 1950 versions show a wide-open mouth on themotor half of the homunculus, and a closed mouth andrather sad expression on the sensory half.2

It is tempting to dismiss this anthropomorphic devel-opment as an artistic whim or amusement. Whilst laterrelegating homunculi to the status of cartoons and aides-memoires for students,23 at least initially the drawingswere a serious endeavour, confirmed by comments suchas that "certain inaccuracies in this figurine are correctedin the text"'-comments which preclude a frivolousintent. Not only was at least the first homunculus there-fore a carefully thought out device, but as a consequenceit could provoke strong reactions. Thus the concept ofthe homunculus was roundly castigated by Walshe:"even today cortical cartography is eagerly pursued asnew modes of electrical stimulation uncover fragments ofelectrical excitability in new cortical territories. Nor arethe moderns content with maps, for homunculi and sim-iusculi have now made their horrid appearances, linealdescendants of Lewis Carroll's Jabberwock, purporting todepict the fair face of nature, but in fact achieving some-thing quite unnatural".'9 It is ironic that Walshe, too,imbues the homunculi he so dislikes with personality, inthis instance, horrid.

Noteworthy is Walshe's reference to cartography, sincethis alludes to one of the functions of such drawings: torepresent the link between points on the surface of thebody with areas within. The essence of all such drawingsis that they are forms of maps, which represent how onecollection of points is linked to another.'0 Maps, however,are designed to be accurate as well as informative, andapart from the paucity of information available particu-larly in humans, there are formidable cartographic diffi-culties in using a device such as an homunculus as a typeof map. These difficulties include two-dimensional repre-sentation of diverse, three-dimensional information bothin the periphery and in the brain, the representation ofmultiple and sometimes overlapping images, and simulta-neous representation of bilateral and unilateral data. Theparticular problems and potential misuse of mapping theelectrical activity of the brain have been admirablyreviewed by Binnie and MacGillivray."

It is clear that both scientifically and graphically thereis considerable ambiguity in what Penfield was intendingto illustrate. This produces unease-even the precedingexample of the map fails. Perhaps this is because thehomunculus is a form of representation, and any repre-sentation of cerebral function is also ambiguous. The

definition and nature of representation in science havenever been satisfactorily defined. As Gooddy points out,"representation is at the bottom of so many schemes ofneurological thinking, whether they be clinical or experi-mental"." This is of considerable importance, not leastsince inappropriate representation could actually impedescientific advance. It might even be the homunculus is aninstance of this. Gooddy's conclusion that "A functiondoes not originate in a specific region of brain tissue,where its 'representation' has been traditionally located"is still valid today, but it points to the problem of howbrain function can ever be illustrated. Amongst otheraspects discussed above, it is this unresolvable difficultywhich makes the homunculus an unsatisfactory and per-haps even misleading image.The periphery of the homunculus is an additional

aspect that requires comment. Penfield's homunculus isshown with an outline which encompasses the area ofcortical representation. What exactly does this outlinerepresent, for we do not feel the outline or periphery ofour bodies? As Schilder comments, "...the outline of theskin is not felt as a smooth and straight surface. This out-line is blurred. There are no sharp borderlines betweenthe outside world and the body".23 The homunculus,however, is outlined by an imaginary 'envelope' whichdoes not exist.

Another phenomenon where the border is blurredbetween fact (pathophysiology) and imagination (subjec-tivity) concerns phantom sensations. Some patientsreport that the phantom that follows amputation oftenfades, but it does so in a non-sequential manner. For aphantom limb, it has been stated that: "The sequence ofdisappearing parts follows, with the possible exception ofthe joints, the Penfield-Boldrey homunculus. Those partswhich have large areas of representation on thehomunculus...are the very same parts which have thelongest phantom life. By contrast, those which have mini-mal representation on the homunculus are relativelyshort-lived as phantoms".'4 Whilst this concept has beenrejected for a number of reasons,'5 it has to be acceptedthat newer theories are as tenuous as those that invokethe homunculus. It requires considerable ingenuity toattempt to describe a phantom phenomenon in terms ofphantom representation.

It can scarcely have escaped Penfield's notice that boththe term and the concept of the "homunculus" are old,dating at least since medieval times; they are also strange.The term merely means "little man" or "manikin", andagain it is curious that Penfield and his collaboratorsshould have used this term. A special use for the termseems implied, since, for example, a man portrayed on astreet sign would not be designated a homunculus.Derived from the medieval idea of creating gold frombase metals, the concept of the homunculus in the pastembodied the idea of being able to create a diminutivehuman, a concept familiar to Paracelsus and lateralchemists. Modern psychology has also embraced thehomunculus-the concept of a little person within one-self, having a personal, internal role, and perhaps theinner person with whom one converses in internalspeech: the function of this inner person is to provide anexplanation or interpretation of the outside world-forexample, an inner person that is responsive to one's pain,or to visual images, or other experiences. The innerperson, however, explains nothing, and the usefulness ofthis concept is dubious.'6

Even beyond the human and animal brain, thehomunculus has acquired status, for it has actually beenendowed with teleological attributes. Thus "The grossdistortion of the imaginative 'little man' shows the high

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P-AW

F'giure 5 Photomiicrograph shozving the relationship between sonmatotopic subareas and architectural organisation of the rat sensory cortex, with parts ofthe bodv drawn around the cortical areas to which they project. Welker, 1976. Reprintedfronm Journal of Conmparative Neurology 1976;166: 173-190,with penmission of The Wistar Inistitute Press.

priority that nature has placed on dexterity in the fingers 5 Hassler R, Mundinger F, Riechert T. Stereotaxis in Parkinson syndrome.prioritythat nature has placed on dexterity in the fingers Berlin: Springer Verlag, 1979: (front cover).and in the control of speech muscles. These two func- 6 Creutzfeldt OD. Cortex cerebri. Berlin: Springer Verlag, 1983: 216.tional areas account for almost half the total area of the 7 Cull P. Medical Illustration. In: Jennings S, ed. The new guide to profes-

sionial illustration and design. London: Headline, 1987: 40-43.motor strip! A similar analysis in other mammals shows 8 Gould HJ, Cusick CG, Pons TP, Kaas JH. The relationship of corpus cal-

quite a different allocation of these areas, reflecting a losum connections to electrical stimulation maps of motor, supplemen-tary motor, and frontal eye fields in owl monkeys. J Comparativedifferent set of behavioural priorities".' For the Neurology 1986;247:297-325.

homunculus, science has now yielded to philosophy. 9 Merzenich MM, Kaas JH, Sur M, Lin C-S. Double representation of thehomunculus, ~~~~~~~~~~~~~~~~~bodysurface within cytoarchitectonic areas 3b and 1 in "51I" in the owlPenfield's homunculus was a deceptively simple and monkey (Aotus trivi'rgatus). J7 Comparative Neurology 1978;181:41-74.

yet naive concept. This type of illustration, a form of 1o Merzenich MM, Kaas JH. Principles of organization of sensory-perceptualyetnafvecncept.Thi type of ilustration a form ofsystems in mammals. Pr~ogr Psychobiol Physiol Psychol 1980;9: 1-42.map, was a highly original attempt to portray graphically 1I1 Wall JT. Variable organization in cortical maps of the skin as an indicationthe observations of brilliant and painstaking research and of the lifelong adaptive capacities of circuits in the mammalian brain.

Trends Neurosci 1988;1 1:549-57.one which has had a lasting influence as a mode of repre- 12 Lenz FA. The thalamus and central pain syndromes: human and animalsentation. It is memorable and useful. It has, however, studies. In: Casey KL, ed. Pain and central nervous system disease: the cen-

tral pain syndromes. New York: Raven Press, 1991:171-182.been of limited and even doubtful scientific value, since 13 Pascual-Leone A, Cohen LG, Hallett M. Cortical map plasticity infact and fancy have been confused. Illustration of brain humans. Trends Neurosci 1992;15:13-14.function by projected drawings may best be reserved for 14 Leyton ASF, Sherrington CS. Observations on the excitable cortex of thefunction by projected drawings may best be reserved for chimpanzee, orang-utan and gorilla. Q JExper Physiol 1917;1 1:135-222.those rare instances where true images can be derived 15 Woolsey CN. Organization of somatic sensory and motor areas of the

cerebral cortex. In: Harlow HF, Woolsey CN, eds. Biological and bio-and recorded. An example is the different cytoarchitec- chemincal bases of behavior. Madison: The University of Wisconsin Press,tural subareas that can be discerned on photomicro- 1958:63-81.

16 Adrian ED. Motor and sensory areas of the brain. The physical backgrouindgraphs of the rat sensory cortex. These disjunctive of perception. Oxford: Oxford University Press, 1946:31-47.somatotopic areas, correlating with the projected periph- 17 Fulton JF. Functional localization in the frontal lobes and cerebellutml.

London: Oxford University Press, 1949:129-130.eral body part, allow the different parts to be identified 18 Kaufmann TD. The allegories and their meaning. In: Hulten P, ed. Theand drawn, and a sensory "rattunculus" can be derived Arcim"boldo effect. Milan: Bompiani, 1987:89-109.

2^1 Representation of everything else may best be 19 Walshe FMR. Some reflections upon the opening phase of the physiology(fig 5).2 Representation of everything else may best be of the cerebral cortex, 1850-1900. In: Poynter FNL, ed. The history,served by an unambiguous diagram or words. anzd philosophy of knowledge of the brain and its fuinctions. Amsterdam: B.

M. Israel, 1973:223-4.I am indebted to Dr P W Nathan and Dr D Fish for their most helpful com- 20 Dykes RW, Ruest A. What makes a map in somatosensory cortex? In:ments, and Dr E Whitcombe for drawing my attention to the paper bv Dvkes Jones, EG, Peters A, eds. Cerebral cortex, V7ol 5, Sensory-motor areas andand Ruest aspects of cortical conzniectivity. New York: Plenum, 1986:1-29.

G D SCHOTT 21 Binnie CD, MacGillivray BB. Brain mapping-a useful tool or dangerousThlc .National Hospital for Neurology and Neurosurge, Pschiatr 199255:527-9.Quecn Squarc, London W'CIN 3BG, UK 22 Gooddy W. Cerebral representation. Brail 1956;79: 167-87.

23 Schilder P. The imtage and appearance of the hum"ian body. London: KeganPaul, Trench, Trubner, 1935:85.

24 Simmel ML. On phantom limbs. Arch Neuirol Psychiatry, (Chicago)1 Penfield W, Boldrev E. Somatic motor and sensorv representation in the 1956;75,637-47.

cerebral cortex of man as studied by electrical stimulation. Brain 25 Melzack R. Phantom limbs, the self and the brain. Canadian Psychology1937j60:389-443. 1989;30,1-16.

2 Penfield W, Rasmussen T. The cerebral corltex of man. New York: 26 Dennett DC. Brainstornms. Philosophical essayNs on miind and psychology.Macmillan, 1950:44, 56, 214-15. Hassocks, Sussex: Harvester Press 1979:57-59.

3 Penfield W, Jasper H. Epilepsy and the fiunctional aniatomyii, of the humolani 27 Pugh GE. The biological origin of human values. London: Routledge andbrain. London: J and A Churchill, 1954:105-106; 159. Kegan Paul, 1978:140.

4 Bates JAV. Stimulation of the medial surface of the human cerebral hemi- 28 Welker C. Receptive fields of barrels in the somatosensory neocortex ofsphere after hemispherectomv. Brain 1953;76:405-47. the rat. 7 Comtparative Neuirol 1976;166: 173-190.

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