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From the Archives
Cambridge
The brain's record of auditory and visual experience. A final summary and discussion. By Wilder Penfield and Phanor Perot. Brain 1963: 86; 595696.
The subtitle of Wilder Penfield's paper, written at the age of 72 years, suggests, like the closing bars of Götterdämmerung, the conclusion to a monumental work of outstanding originality but, in Penfield's case, born not out of Teutonic mythology but from experimental neurology. Penfield had dedicated his first classic monograph, written with Theodore Erickson (Epilepsy and Cerebral Localisation, 1941) to John Hughlings Jackson and Charles Sherrington. Later, he gave the fifth Sherrington Lecture in the University of Liverpool (1958). The introduction to this final summary of his life's work, based in part on the Lister Oration (1961) and the Hughlings Jackson Lecture (Montreal, 1961) quotes Jackson: he who is faithfully analysing many different cases of epilepsy is doing far more than studying epilepsy; and almost 100 pages later Penfield closes with the same quotation. The story is of Jackson's dreamy states and of their illumination based on Penfield's observations over a period of 25 years on experiential hallucinations and experiential responses to focal cortical electrical stimulation. He found these to be both simple and complex; in the domains of language, sound or vision; with the emotional conviction of past experience; and, where factual corroboration proved possible, founded on genuine events now recalled. Proustian, therefore, in its scope (and biblical in its resonances of Ecclesiastes 3: 18), this is an account of the cortical substrates for remembrances of past experiences drawn from the times of watching or hearing the action and speech of others, and times of hearing music ... it may have been a time of listening to music, a time of looking at the door of a dance hall ... a time of hearing your father and mother singing Christmas carols. Of no less interest to Penfield were the times of carrying out skilled acts ... or of writing messages and adding figures ... the times of eating or tasting food ... the times of sexual excitement or experienceas well as periods of painful suffering or weepingsince these were all conspicuously absent from the experiences described by patients in this our last exhaustive survey.
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From a personal series of 1288 procedures in 1132 individuals studied between 1934 and 1961, Penfield and Perot identified 40 (7.7%) cases with experiential responsesall resulting from stimulation of the temporal lobe using a 1.5 mm square silver ball electrode providing square-wave pulses of 25 ms at 40100 Hz, 15 volts, delivering a stimulus current of 50500 micro-amperes. Of these, 24/40 had previous experiential seizures and 16/24 had a faithful reproduction of those experiences during electrical stimulation; a further 29/520 had experiential seizures but no peroperative experiential responses. Thus, Penfield and Perot could draw on 93 sets of observations in 69 different individuals. Many of these cases had previously been described in publications with younger colleagues: Maitland Baldwin, William Feindel, Herbert Jasper, Brenda Milner, Sean Mullan, Theodore Rasmussen, Lamar Roberts and Keasley Welch. In the auditory domain, voices were elicited from 46 different cortical points, and sounds from 17. Precautions were taken to establish the authenticity of responses by posing questions without stimulation, stimulation without questions, and prolonged stimulation before springing the question. Many heard music.
Case 4 confirmed, yes, it is "White Christmas"; for case 5, stimulation at point 23 elicited a tune that the patient hummed: the timing was just what one would have expected, no faster and no slower. Miss Stanley, the operating room nurse, recognized the tune as "Rolling Along Together"; case 6 always heard "Hush-a-bye, My Baby" as if in a church or convent in her seizures, and electrical stimulation reproduced music: a funny little piece, the same lullaby ... something heard on the radio ... the theme song of a children's programme; case 6 started humming to himself in attacks and then the music would continue as a familiar folk song or an orchestra playing classical music; case 9 heard a sound in the distance like people singing ... a bunch of old folks in the background ... probably hymns; case 10 was reminded of a song that he had heard before, a popular one on the radio, but he did not know the name of it; for case 11, the music was an orchestra or an organ; case 13 heard a girl or a woman singing but I am still unable to get the tune. It came from either a record player or a radio; case 14 felt that the song he heard seemed to continue from the words of the surgeon who recorded his responses; during stimulation, case 29 was trying to find the name of a song and remembered a piano there and someone was playing ... it is a song I have sung before but I cannot find out quite what the title of the song is ... yes "Oh Marie, Oh Marie"someone is singing it. I cannot recognize the voice ... again, "Oh Marie, Oh Marie" ... it is a theme song on a radio programme. The programme is called "Life of Luigi" and he then demonstrated the experience by singing the well known refrain to Dr Sears; in case 31 stimulation of point 31 triggered that baby song"The War March of the Priests", to be found on the other side of the recording of the "Hallelujah Chorus"; case 32 heard her mother and father talking and singing Christmas carols; for case 37 the experiential content resulting from stimulation of point 14 was that music from the stage hit Guys andDolls.
In the separate category of cases in whom experiential hallucinations occurred without corresponding stimulation responses, on getting up to go to the bathroom at night, case 45 heard familiar music coming from the radio in the living room downstairs, but with undecipherable words; case 46 heard an orchestra playing I'll Get By and You'll Never Know, familiar from the radio and dance halls; in case 47, the attacks were associated with words set to music, similar to a radio commercial or an advertising jingle.
In putting their cases into perspective, Penfield and Perot drew on a comparatively modest literature describing musical sensations during temporal lobe seizures. Formulating their own conclusions concerning auditory experiential hallucinations and responses to electrical stimulation, Penfield is the functional anatomist and interpretative physiologist, rooted in the significant works of 19th and early 20th century neurology written by Thomas Buzzard, Alfred W. Campbell, Constantin von Economo, Wilfred Harris, David Ferrier, William Gowers and (John) Hughlings Jackson, that he quotes. His observations led him to conclude that the primary auditorysensory cortex lies on the anterior transverse temporal gyrus of Heschl within the sylvian fissure. The region that gives rise to auditory epileptic experiences and electrocortical experiential responses is the superior temporal convolution, with some differences between left and right: there is a sharp functional frontier between the sensory and the interpretative areas ... in the auditory cortex (the electrode may elicit) a ringing, humming or rumbling ... but then, if the electrode is moved only a few millimetres away into the neighbouring cortex around these sensory areas, a response of a totally different order of neuronal organisation may result. There is no longer a sound but a voice, no longer a rumbling but music. As expected from Sherringtonian principles of physiology, these auditory experiential responses arising from electrical stimulation of the associative cortex were subject to facilitation or inhibition by appropriately placed prior stimulation.
Dr Feindel recalls, laconically, thatfar from representing a "final summary"Penfield was to be found drawing on his pipe, wrapped in a woollen Witney blanket and draped around a 2-bar electric heater whilst working on his next manuscript (Conditioning the uncommited cortex for language learning: Brain 1965: 88; 787798), when they both attended the 700th anniversary of Merton College, Oxford on a quintessentially chilly April day in 1964. In the event, he went on to publish another 40 papers and four books, including his autobiography (see above), over the next decade.
Born in the year that Charles K. Mills reviewed the localization of the auditory centre based on clinicopathological correlation (Brain 1891: 14; 465472), and living to see the introduction of anatomical localization through computed tomography, Penfield combined an astute observational and experimental approach to provide the classical account of functional localization for hearing the sound of music.
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