From the Archives
The frontal lobe in man: a clinical study of maximum removals. From the Department of Neurology and Neurosurgery, McGill University, and the Montreal Neurological Institute. By Wilder Penfield and Joseph Evans. Brain 1935; 58: 115–133.The authors introduce their study of three individuals in whom a substantial part of one frontal lobe is removed with a cautionary note: the opportunity provided by investigating the effects of neurosurgery may be confounded by ‘bilateral representation of many cerebral processes which take place in this terra incognita’, and by the disadvantage of including examples of cerebral tumour since these may have distant effects through displacement and infiltration. Thus, although cases with epilepsy are best, those with a very wide tumour resection—extending well into normal brain—may yet be informative. That said, ‘it may be urged that to destroy a delicate instrument is not the best way of studying its function’.
Case 1, described in most detail, had a right frontal oligodendroglioma. The history was available from childhood and consisted of Jacksonian seizures, occurring in short series on five occasions over a 20-year period but with a slight increase in frequency prior to surgery at the age of 43 years. Pre-operative assessment by Dr Colin Russel noted bilateral papilloedema and signs of a left hemiparesis: ‘mentally [she] was not up to her own standard in looking after household arrangements’. Wilder Penfield operated, late in 1928, removing a substantial part of her right frontal lobe. An artist (whom we know to have been Harriet Blackstock, a former student of the great Max Brödel; see Brain 2006: 129; 820–824) was present, and recorded the procedure (Figs 1 and 2). The patient was conscious throughout, apart from during a brief but brisk haemorrhage, and ‘at the end of 6 h ... apologized for having made so much trouble!’. She returned home and at first appeared well but, after nearly 2 years, the symptoms returned and Harvey Cushing operated on the tumour recurrence—without much success, for she died 6 months later from haemorrhage into the residual tumour mass. Autopsy, performed by Dr Carl Rand of Los Angeles, showed an expanded right hemisphere (minus its anterior pole) due to tumour (Figs 3 and 4). Case 2 suffered epilepsy secondary to a left frontal cicatrix resulting from trauma. Penfield removed a large portion of that frontal lobe in November 1929, under local anaesthesia: the patient was muddled during the first post-operative week and developed a partial right hemiparesis, but these deficits improved thereafter. Case 3 underwent right frontal lobectomy, in 1931, for removal of a post-traumatic cystic cicatrix producing epilepsy of focal onset; re-operation proved necessary 2 days later for recurrent haemorrhage, but his seizures were subsequently well controlled.
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The point of this paper is not surgical braggadochio but—notwithstanding the contribution of symptoms directly attributable to the disease processes in these three cases—to record the subtle changes that occur in people who have lost a frontal lobe. Therefore, their pre- and post-operative social and neurological functions are of great interest. And now, Dr Penfield drops a bombshell. For Case 1, described in most detail, on whom he himself operated and now reports with post-mortem illustrations was Ruth, his only sister.
Later, Penfield devoted a chapter in his autobiography, No Man Alone, to ‘My Sister’. He was urged to operate on Ruth by his neurosurgical colleagues Eddie Archibald and Bill Cone; Colin Russel, who provided neurological counsel, agreed with this decision. For the first time they used the arrangement of drapes allowing communication under local anaesthesia learned from Otto Foerster in Breslau. It was a harrowing experience since in attempting to remove the last part of the tumour deep in the mesial frontal region, and against Cone's advice, Penfield caused ‘brisk haemorrhage’ (William Feindel, to whom we are indebted for personal recollections of this poignant episode in Penfield's neurosurgical career and certain factual details, rephrases this as ‘massive bleeding’).
‘My instinctive reaction was to withhold this case from publication ... but the close bond of sympathy that had existed between us makes it possible for me to evaluate the effect of the loss of the frontal lobe upon her personality and her mental capacity ... if she were alive I am sure she would approve of such an analysis in the hope that it might help others’. Speaking 3 h after surgery, Ruth was again keen to impress upon Colin Russel her appreciation to everyone in giving up their time, and how afraid she had been of causing distress by making an exhibition of herself ... ‘when I remarked that the only exhibition I had seen was one of the best of courage it had been my fortune to witness, she expressed her gratitude so nicely that one could not help wondering how much the frontal lobe had to do with the higher association processes’. Ruth had undergone the most extensive resection of the three cases, providing the most intimate observations on behaviour before and after frontal lobectomy. Although superficially resuming her duties as wife and mother of six children with greatly increased efficiency, Ruth was conscious of not being alert mentally: ‘each time I feel encouraged, I do a series of very stupid things’. Whilst not lacking in personal care, and with no change in memory, insight, conversation or sense of humour, she did not discipline her children and household administration proved difficult. Loss of the right frontal lobe had resulted in an important defect—a lack of capacity for planned administration: ‘fifteen months after operation, she had planned to get a simple supper for one guest (WP) and four members of her own family ... when the appointed hour arrived the food was all there, one or two things on the stove, but the salad was not ready, the meat had not been started and she was distressed and confused by her long continued effort alone ... the element which made such administration almost impossible was the loss of power of initiative ... she had become incapable of discerning for herself possible courses of action so that she might chose. If others presented the possibilities she made up her mind quite easily’.
Against this background of informal analysis, Penfield and Evans perform a more systematic clinical evaluation of Cases 2 and 3, noting the difficulty of separating the confounding effect of improved seizure control from that of frontal lobectomy. Case 2 showed an ‘ability to think better, act more quickly and [be] less irritable and quarrelsome ... [this] should not be taken to mean that we consider frontal lobectomy would benefit a normal individual’. Within a few months of surgery, Dr David Slight found Case 2 to have no demonstrable mental changes, apart from some difficulty in holding figures in his head whilst playing a game called ‘five hundred’ and at Bridge (‘a game which calls, no doubt, for a certain limited type of memorization and computation!’), but with a marked change in attitude: ‘previously he was very antagonistic toward people and religious topics and such like, whereas now he finds himself more controlled in approaching and discussing such matters’. And although his mother ‘admits that he may have shown too little initiative ever since his injury ... the father [head groundsman for McGill University] states that "he never had a job that I didn't get for him". He should have added "since the accident" for he had had enough initiative to find his way to England at the age of 16, and had secured himself a job there. To sum up: this is a likeable fellow, a good workman and a useful citizen. It is quite certain he will never be a revolutionist. He has lost something that psychometric examination does not evaluate. He has lost initiative; not all of it, but much of it’. Vestibular function was studied in much detail and found to be normal; and meticulous examination of sensation revealed a ‘suggestive error in spot finding on the right leg by the right index finger ... slight unexplained error in recognition of grades of sandpaper, fifth finger right and third finger left ... left hand unsupported recognized the differences in weight less readily than the left ... diminished acuity in recognition of figure writing in the right palm’. Case 3 had entirely normal special sensory, auditory and vestibular functions, and no psychological or behavioural deficits could be discerned on examination or from knowledge of his social and professional activities.
So, for Penfield and Evans (who was later chief of neurosurgery at the Universities of Cincinnati and Chicago) ‘large amputations of the frontal lobe, if the precentral gyrus be left intact, produce surprisingly little disturbance of function which can be detected by ordinary methods of examination ... neurologically ... and by the ordinary psychometric tests each would have to be judged normal although neither (sic) would rank very high ... each was very good-natured and co-operative which may in some cases perhaps be an evidence of lack of initiation of ideas ...we have been told by relatives that removals of a very large area of frontal lobe with included neoplasm have resulted in marked improvement in the patient's temper’. And their conclusion is that ‘maximum amputation of right or left frontal lobe has for its most important detectable sequel impairment of those mental processes which are prerequisite to planned initiative’.
Building on the work of Professor Leonardo Bianchi from Napoli (La meccanica del cervello e la funczione dei lobi frontale, 1920; English translation 1922), Penfield presented these cases to the 1935 International Congress of Neurology in London (although he is missing from the photograph of the Neurosurgical group), at which Richard Brickner also reported on a patient in whom Walter Dandy had removed the frontal lobes, and Carlyle Jacobsen described the effects of bilateral frontal lobectomy in two chimpanzees, Clyde and Becky. Antonio Caetano deAbreu Freire Egaz Moniz—Professor of Neurology, contributor to the introduction of cerebral angiography, Minister of Foreign Affairs, Ambassador to Spain, later Nobel laureate and near-fatal victim in his office of a gun-toting schizophrenic—listening in the audience, returned to Portugal and, on November 12, 1935, persuaded his neurosurgical colleague Almeida Lima to make a lesion in the frontal lobes of a psychotic individual, thereby initiating the discipline of psychosurgery. Donald Hebb, with whom Penfield later collaborated, considered that ‘Penfield changed the whole doctrine and theory of frontal lobe function and the basis of so-called frontal lobe signs’ motivated as he was by the dictum that ‘bad brain is worse than no brain at all’.
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