TY - JOUR
AB - Abstract Research on memory has been a major focus in the neurosciences over the past decades. An important advance was achieved by Wilder Penfield at the Montreal Neurological Institute, who reported from the 1930s to the 1950s about experiential phenomena induced by electrical brain stimulation in humans, implying neuronal causation of memory. Since then, neuroscientists have addressed the topic of memory from a range of subdisciplines; however, these reports by Penfield and his group as well as those on patient H. M. by Brenda Milner at the same institution continue to be referenced as groundbreaking. Further experimental work by Nobel laureates Eric Kandel and John O’Keefe, as well as by Edvard and May-Britt Moser related Penfield’s patient documentation to experiential phenomena. However, our reassessment of Penfield’s original patient documentation questions the stance that he had uncovered the “storehouse of memories.” Human memory must be regarded more as context sensitive and as representative of an active reconstructive process, than as a simple recording of events. Hence, strategies aiming at naturalizing all phenomena of mind (including memory) to cellular and molecular mechanisms cannot convincingly refer to Penfield’s electrophysiological studies alone as evidence that memories are solely caused by neuronal firing patterns. brain stimulation, consciousness, cortical organization, memory, temporal lobe Introduction Extensive parts of our idea of memory as a neuronal record of the stream of consciousness have been influenced by studies in psychiatry, neurology, and clinical neuroscience during the last 60 years (Loftus et al. 1978). These assumptions increasingly led to reductionist concepts that aimed at naturalizing all phenomena of mind (including the important higher function of memory) to cellular and molecular mechanisms of the human nervous system (Nitsch 2012). The wider history of the naturalization of the higher “actions” or “functions” in the human brain reaches back at least 250 years, and is often traced to the phrenological works of the Austrian anatomist Franz Joseph Gall (1758–1828) (Hagner 1997). Modern discussions on whether memory functions could be localized in structural areas of the human brain have been related to the clinical neurophysiological work of Wilder Penfield (1891–1976) at the Montreal Neurological Institute (MNI) of McGill University in Quebec, Canada since the 1930s (Snyder and Whitaker 2013; Feindel and Leblanc 2016). Ultimately, the behavioral studies of Brenda Milner (b. 1918) together with William Beecher Scoville (1906–1984)—in which they defined memory as a “hypothetical record of the stream of consciousness” (Penfield and Mathieson 1974)—terminated, at least for the most part (Halgren et al. 1978) a controversial debate over the localization of human memory function (Milner 1977; Xia 2006). Penfield encouraged Milner to take up her PhD research at the MNI—under the supervision of Donald O. Hebb (1904–1985)—and to conduct research into memory and cognition on many of his patients (Milner et al. 1998). Together with Scoville, she showed that their bilaterally hippocampus-ablated patient “H.M.” (Henry Molaison; 1926–2008)—who has since become the paradigmatic case for memory studies in cognitive and clinical neuroscience (Dossani et al. 2015)—displayed a persisting anterograde form of amnesia after the neurosurgical removal of both hippocampi and adjoining structures (Scoville and Milner 1957; Augustinack et al. 2014). In parallel, Penfield reported on 2 patient cases of unilateral removal of the anterior–lateral temporal neocortex and the hippocampus, which showed severe memory deficits related to pathological sclerosis (resulting in a bi-lateral functional loss of the hippocampi (Feindel and Leblanc 2016). Milner analyzed the specific instances of learning processes in H.M. and demonstrated a relationship between the extent and location of the structural lesion and resulting memory impairment (Milner and Klein 2016). She followed up with the patient over 3 decades, and his loss-of-function was regarded as the most compelling proof for the existence of a temporal lobe memory system (Squire 2009). Millennium Nobel Prize winner Eric Kandel (b. 1929) summarized the common view on these findings as follows. From her systematic studies of H.M., Milner extracted 3 important principles of the biological basis of complex memory. First, memory is a distinct mental function, clearly separate from other perceptual, motor, and cognitive abilities. Second, short-term memory and long-term memory can be stored separately. Loss of medial temporal lobe structures, particularly loss of the hippocampus, destroys the ability to convert new short-term memory to new long-term memory. Third, Milner showed that at least one type of memory could be traced to specific places in the brain. (Kandel 2004) As a result of this research, most neuroscientists today endorse the interpretation by Eric Kandel and Larry Squire (b. 1941), who depicted the historical development of learning and memory research as a paradigmatic example for how the removal of scientific barriers between the molecular and cellular level on the one hand and the biology of cognition on the other hand had framed a clear “success-story” (Kandel and Squire 2000). They claim that such a synthesis is apparent in the study of memory storage and synaptic plasticity, which would have led to a scientific unification between psychological and neuro-psychiatric research. Kandel’s notion of a “new biology of mind” therefore proposes a naturalistic reduction of psychiatry which even includes psychoanalysis to underlying neuronal mechanisms (Kandel 2005). This concept made neuroscientific memory research a pivotal societal issue as well (Klafki et al. 2006), and enormous funding programs have been established to solve the problem of memory loss in neurodegenerative disorders (Insel et al. 2015). It has to be noted, however, that a critical reappraisal of the analysis performed on H.M. raises serious doubts that lesions to the temporal lobe alone explain the patient’s cognitive deficits. Likewise, the reproducibility of the psychological assessments performed by Suzanne Corkin (1937–2016) during H.M.’s lifetime has been taken into question (Dittrich 2016). Moreover, there is considerable scholarly debate about the originality of Penfield’s contributions to the field of neurophysiological localization of the higher psychological functions in the human cortex as well as about the operational research approaches Penfield chose in his neurological and psychiatric patients (Kolb and Teskey 2012; Guenther 2016). This has led to a new view of memory as an active reconstructive process, no longer limited to electrophysiological recordings alone (Roediger and DeSoto 2015). In our reassessment of the historical record of the primary patient data maintained in the archives of the MNI, as well as through direct communication with eye witnesses of Penfield’s research activities, we discovered remarkable inconsistencies between operational protocols of brain stimulations and data sets published at a later point in time. It appears that, contrary to Penfield’s claims, brain stimulation in man fails to induce full memory, including its semantic content, and only demonstrates that the brain is a necessary condition for “producing” memory (Penfield and Mathieson 1974). Materials and Methods In this study, we collected original patient data sets from the Historical Archival Collections at the MNI. These original case reports and neurophysiological documentations of the cortical stimulation experiments were contrasted with published patient records and case histories. We have scrutinized historical operation records, patient files, and published articles, primarily from the archives of the MNI and the Allan Memorial Institute (AMI) in Montreal, Quebec, as well as autobiographical material from neuroscientists and psychiatrists who witnessed this crucial period. We assessed the classification of “experiential phenomena” induced by electrical stimulation as proof of the neuronal causation of memory. Methodologically, our study was limited in several respects: Since Penfield died in 1976, he could not be interviewed personally, although it was still possible to assess his written experimental records and published autobiography. However, we were able to speak with William Feindel (before his death in 2014), Milner, and Doris H. Annear from Penfield’s operation theater nursing team at the MNI to gain first-hand information from them. The historical method of data acquisition does not lend itself directly to reproducible and statistical validation, yet it allows for evidential appreciation of the development and growth of modern experimental memory studies and permits an informed critique of the widespread influence and reductionist conceptions of memory in the history of ideas in the modern neurosciences. Naturalizing Memory: “Gain-of-Function” by Electrical Stimulation In addition to his own groundbreaking work on the differentiation of the sensory-motor homunculus of the human cortex (Penfield and Boldrey 1937), Penfield was instrumental in aligning his neurosurgical explorations with psychological and psychiatric research on cognition and memory (Penfield and Boldrey 1937; Guenther 2016). Already years before the report on patient H.M., Penfield also performed “gain-of-function” studies, using electrical stimulation of brain structures during operations on conscious patients (Gavrus 2015) based on a neuro- and psychosurgical paradigm that he had learned while staying with Otfrid Foerster (1873–1941) in Breslau during his European research period in the late 1920s (Foerster and Penfield 1930; Stahnisch 2008). The first detailed and comprehensive report of verbal accounts elicited by electrical stimulation was given in a Master’s thesis of one of Penfield’s research fellows, Maitland Baldwin (1918–1970) in 1952. Those accounts resulted from stenographs made by a secretary, who was present in the operation theater and noted the operator’s (not the patient’s!) summaries or repetitions of the patient’s wordings. Baldwin classified these accounts as involuntary recollections, illusions, psychical hallucinations, and emotions, according to their potential realistic content. One example, classified by Baldwin as involuntary recollection, is characteristic for the present series of electrical stimulations of the temporal cortex, as reported about patient T.S.: Point 14 was stimulated 9 times with a current of 5 V. This voltage is higher than the voltage threshold for the postcentral gyrus. During the first 3 of these stimulations he said he felt as if he was going into an attack or answered, “Nothing.” In the second and third there was an electrographic abnormality as noted above. In the fourth there was a “flattening” of the electrographic record, and after about 10 s the patient said, “I feel as though I was in the bathroom at school.” He had not been warned that stimulation was in progress. During the fifth stimulation he said, “Nothing”, then added, “Slight blurring on the street corner”. When asked where, he said, “South Bend, Indiana—Jacob and Washington.” When asked about it, he said he seemed to be looking at himself at a younger age. The sixth time he said, “Nothing.” This was his first response at the stimulation, but it was quickly followed by the statement, “I feel as though I am going into an attack.” When asked why, he said, “That music from the stage hit, “Guys and Dolls.” When asked to name the song, he was unable to name it. He added that it was more like it was “when I was listening to it.” It was an orchestration. “I seemed to be there.” The eighth and ninth stimulations were negative. (Baldwin 1952) Baldwin classified this verbal account upon electrical stimulation as an involuntary recollection, since, in contrast to illusions or psychical hallucinations, the verbal account could be related in part to documented events in the patient’s past: This boy had lived in South Bend, Indiana, and had recently seen the musical comedy “Guys and Dolls.” The music and the scene were familiar to him. He was aware of their familiarity. This feeling of reminiscences was accompanied by a sense of participation. Thus, he recognized the music and the scene in South Bend as fragments of past experiences. At the same time, he was conscious and knew that he had not voluntarily summoned these memories to the foreground of his consciousness. The stimulating current has done this for him. Apparently, the pathway stimulated was also available to voluntary interpretation, because he knew that both the song and the scene were being played only for him and were not from the immediate external environment. Although categorized as a form of involuntary recollection, there was supportive evidence that the patient had experienced some of the response content in his past. (Baldwin 1952) It is important to note, however, that the verbal account was not solely elicited by the electrical stimulation, but also by questions raised by the operation team. The responses elicited from the stimulation alone (at one point, no. 14) resulted in a variety of verbal responses, ranging from “Nothing” to “I feel as though I was in the bathroom at school” to “Slight blurring on the street corner.” All of these personal accounts did not contain meaningful memory content which could be referred to the patient’s past experience. Only when asked, the patient framed part of these accounts into his past context by answering “South Bend, Indiana—Jacob and Washington” and “That music from the stage hit, ‘Guys and Dolls’,” as well as his interpretation that “he seemed to be looking at himself at a younger age.” Evidently, it was the conscious patient’s semantic ability, not the electrical stimulation, which provided the respective and meaningful memory content in this situation. Nevertheless, based on these types of operation reports and their early interpretations, Penfield already postulated during his Montreal Gordon Wilson lecture on “The Mechanism of Memory” in 1950 the existence of a “storehouse of memories” within the brain: It requires no great effort of introspection to discover the fact that one can, at will, select from a very large number of remembered items: a familiar piece of music, a landscape, a poem, an experience. It stands to reason than that there must be somewhere in the central nervous system a storehouse of memories. Each memory must obviously have its own peculiar neurone pattern, a pattern that is not inborn but acquired. (Penfield 1950) Penfield maintained this view throughout his career, and summarized his concept in a sketch drawn in 1973 (Fig. 1). This concept that electrical stimulations in certain brain areas produce experiential phenomena, which represent quasi “taped memories” (Penfield 1938) has been a dominant research principle until very recently. Figure 1. View largeDownload slide Penfield’s sketch of the tape recorder model of memory as part of the stream of consciousness in the hippocampi 1973. Reproduced from: Wilder Penfield: his legacy to neurology. Memory mechanisms, Milner B, CMAJ June 18, 1977 116 (12) 1374–1376; by permission of Canadian Medical Association Journal. This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Figure 1. View largeDownload slide Penfield’s sketch of the tape recorder model of memory as part of the stream of consciousness in the hippocampi 1973. Reproduced from: Wilder Penfield: his legacy to neurology. Memory mechanisms, Milner B, CMAJ June 18, 1977 116 (12) 1374–1376; by permission of Canadian Medical Association Journal. This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Stimulation protocols and maps by Penfield and Perot (1963) In 1963, Penfield—together with Phanor Perot (1929–2011)—reported an overview on forty patients who underwent intra-operative instances of brain stimulation in a conscious state between the 1930 and 1950s. This report included cases described earlier by Baldwin, now classifying all responses (such as involuntary recollections, illusions, psychical hallucinations, and emotions) as “experiential phenomena” to represent the hallmark of memory. The previous differentiation of the different types of verbal accounts—related to proven past experience or not—was no longer upheld. Moreover, when comparing the published information on individual cases with original patient documentation maintained at MNI archives, there are considerable discrepancies as exemplified for the case of another patient, called D.F.: The report given in the paper (Penfield and Perot 1963) is as follows (see also the published stimulation map, Fig. 2): 23. Stimulation produced a slight substernal sensation. 24. Repeated. “I hear some music.” Repeated without warning, “I hear music.” 25. Repeated without warning. “I hear the music again. It is like the radio.” When asked what tune, she said she did not know but that it was familiar. 26. Repeated again without warning. The patient said, “I hear it.” The electrode was kept in place and she was asked to tell us about it. She then hummed the tune. When asked, she said she never noticed that before an attack. … Stimulation at 3 points in the vicinity of point 23 caused the patient to hear the same tune. She hummed it quite distinctly. Miss Stanley, the operating room nurse, recognized the tune as “Rolling Along Together.” The patient agreed that this sounded like the words in the song. On inquiry, the patient said it was not a question of being made to think about it, but that she actually heard it. When she accompanied the music that she heard, the timing was just what one would have expected, no faster and no slower. This suggests [sic] that the bombardement [sic] of electrical pulses from the electrode can only cause the stream of experience to move forward in the original tempo. (Penfield and Perot 1963) Figure 2. View largeDownload slide Stimulation map of case D.F. as shown in Penfield and Perot (1963). Reproduced from: The brain's record of auditory and visual experience. Penfield W, Perot P. Brain 1963 86: 595–696; by permission of Oxford University Press. This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Figure 2. View largeDownload slide Stimulation map of case D.F. as shown in Penfield and Perot (1963). Reproduced from: The brain's record of auditory and visual experience. Penfield W, Perot P. Brain 1963 86: 595–696; by permission of Oxford University Press. This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Interestingly, in contrast to the original stimulation protocol (Fig. 3), only a fraction of this report was displayed by Penfield and Perot (1963), although the patient produced various other verbal expressions, but obviously not in a meaningful context. It is, however, important to note, that electrical stimulation also results in either an absence of verbal expressions or expressions that appear to be meaningless. It is thus difficult to follow conclusions such as the following: It is often evident that each stimulation leaves behind a facilitating influence so that the same response follows each stimulation and this facilitation may cause the same response to follow stimulation at 1–3 cm distance. This is illustrated by Case 5, D. F. She heard the same song played by an orchestra and beginning at the same place in the music when a certain point was stimulated more than 10 times. Fifteen minutes elapsed between the first stimulation and the second which was carried out without warning her. There were no other experiential responses in this case. But the same music was produced at 3 points quite near the original spot. (Penfield and Perot 1963) Figure 3. View largeDownload slide Original stimulation protocol of case D.F. Reproduced from: Case History, Montreal Neurological Institute, 1949, No. 49-5313. Reproduced by permission of the MNI (Copyright holder). This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Figure 3. View largeDownload slide Original stimulation protocol of case D.F. Reproduced from: Case History, Montreal Neurological Institute, 1949, No. 49-5313. Reproduced by permission of the MNI (Copyright holder). This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Penfield and Perot interpreted their findings as a proof for the fact that repetitive stimulation of one point or its close vicinity elicits the same memory content (Penfield and Perot 1963, p. 683). However, an in-depth comparison with the original stimulation map (Fig. 4) shows clearly that the original stimulation protocol (Fig. 3) did not support this repetitive account by stimulation at the same point. In fact, simulation at point 23 initially “produced an aura but not strong” and 4 repeated stimulations thereafter at point 23 resulted in some report on music (the word “orchestra,” however, is not part of the initial report, nor were there 10 stimulations at the same point), but later stimulations at the same point induced a “funny feeling.” Moreover, the patient reported to have heard music, on request hummed the tune, and after identification of the song by a member of the operating team due to this humming, she agreed “that this sounds like some of the words in it.” Evidently, the interpretation from third-party information was needed to provide some contextual meaning to the experiential phenomenon reported by the patient. What was claimed to be a specific, deep and full memory of a piece of music turns out to be a fragment of some phenomenal information, which is inconsistently elicited at one given point. Figure 4. View largeDownload slide Original stimulation map of case D.F., female patient aged 26 with focal epilepsy, operation: removal of anterior end of temporal lobe 1949. Reproduced from: Stimulation Map, Montreal Neurological Institute, 1949, No. 49-5313. Reproduced by permission of the MNI (Copyright holder). This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. Figure 4. View largeDownload slide Original stimulation map of case D.F., female patient aged 26 with focal epilepsy, operation: removal of anterior end of temporal lobe 1949. Reproduced from: Stimulation Map, Montreal Neurological Institute, 1949, No. 49-5313. Reproduced by permission of the MNI (Copyright holder). This image is not covered by the terms of the Creative Commons licence of this publication. For permission to reuse, please contact the rights holder. A similar critical perspective has already been taken by the American-British neuroscientist and Nobel laureate John O’Keefe (b. 1934) and the American psychologist Lynn Nadel (b. 1942). They stated that “the representations of physical occurrences in the right hippocampus […] form the basis of what is generally referred to as long-term, context-specific memory for episodes and narratives [emphasis by the authors]” (O’Keefe and Nadel 1978). This understanding of the context-specific dimension and thus the semantic reconstructive nature of memory is in apparent contrast to the passive “storehouse” metaphor of memory by Penfield. It appears that the neurosciences of memory can merely decipher the representations of physical occurrences as a basis for this semantic reconstructive ability of human cognition, not the storehouse of memories. There is also considerable concern about the specificity of experiential phenomena elicited by electrical stimulation in defined cortical structures. Given the assumption that specific “ganglionic patterns in the temporal cortex” encode specific memories, it is difficult to understand why stimulations within the vicinity of an initial stimulation point could be explained by facilitation. In a compartment of “1–3 cm distance,” an estimated number of tens of thousands of neurons is located however; a stimulation in such an area results in a variably similar, but also different experiential phenomenon. Hence, the “recording mechanism for memories of events” as postulated by Penfield and Mathieson (1974), appears to be an unspecific response upon activation of large groups of neurons, which elicit fragmentary aspects of undefined past events as patients have experienced. Evidential constraints of Penfield’s Wilson Lecture (1950) Thus, revisiting the clinical work of Penfield—on what he called experiential phenomena—reveals that the actual results obtained from electrical stimulation studies of the brain (including the concomitant verbal remarks noted from his patients) are far less conclusive, than his firm assertions made during his Gordon Wilson Lecture in 1950 (Penfield 1950). This is not merely due to the fact that only a minor proportion of electrical stimulations in the temporal lobe could elicit any kind of response (about 7%, according to his own equation in Penfield and Perot (1963)), but result from the fact that no consistent response of defined experiential phenomena could be observed upon stimulation of an individual stimulation point no full memory repertoire could be elicited, but rather fragmentary aspects of the experienced past were reported and no record of the stream of an individual’s consciousness could be taken from the patient’s stimulation records. Penfield’s “storehouse” metaphor refers to the presence of data storage systems in computer technologies, from which an individual was able to retrieve a set of information (Fig. 1) (Grote and Stadler 2015). The structure of this information, in Penfield’s terms, however, was based in the concepts of phenomenal information, such as familiar pieces of music, landscapes, poems, and individual experiences. The idea behind the “storehouse of memories” is obviously the assumption that defined memories, such as a contextual set of information about a past event, had their “peculiar neurone patterns” (Millett 2001). It reflects on the idea that the large variety of input, which the brain computes during its daily work, was integrated in one common medium, namely, the variable rates of neuron firings, as American philosopher of mind John Rogers Searle (b. 1932) has intriguingly pointed out and assessed (Searle 1984). Penfield himself was strongly criticized by later contributors for having localized memory only in the temporal lobe. The point to be made here, nevertheless, is to unmask the underlying reductionist concept of naturalizing memory as a whole, when Penfield for instance interpreted his findings from electrical stimulations as an empirical data set within the neurosciences: Experience with electrical stimulation of the human brain makes it apparent that this storehouse is to be found in the neuronal connections of the right and the left temporal cortex. (…) It is obvious that there is beneath the electrode a recording mechanism for memories of events. But the mechanism seems to have recorded much more than the simple event when activated it reproduces the emotions, which attended the original experience. What is more, the ganglionic mechanism (ganglionic signifies a group of neurons: neuronal mechanism [authors’ explanation]) continues to add to itself the memory of emotions which attend the recollection of the event and the substance of the man’s reasoning regarding the significance of the event. (Penfield and Rasmussen 1950) Following Penfield’s conclusions, neuronal firing encodes for both the recollection of a set of data about a past event, stored as a set of physical information, yet also “the emotion that the individual “felt” at the time of the original experience” as a set of phenomenal information, as well as the reasoning regarding the significance of the event and “the deductions,…, that he made concerning the experience,” comprised of semantic information, such as bringing the physical and phenomenal information under categories of “true and false” (Penfield 1950). These conceptual statements made by Penfield unravel the underlying strategy of naturalizing memory, possibly best characterized as naïve physicalism, as expressed by Searle (1992) and more recently by German analytical philosopher Markus Gabriel (b. 1980; Gabriel 2017). This physical representation of a contextual set of information which sees semantic content as represented in a pattern of neuronal firing is a perfect example of psychiatrists’ and neurologists’ conviction that “the power of the physical model of reality (…) is so great that it is hard to see how we can seriously challenge naïve physicalism” (Searle 1984). References to Penfield’s Concept of the Storehouse of Memories To date, the article by Penfield and Perot (1963) has been cited more than 1500 times and has attracted attention from various perspectives over long periods of time (Compston 2005); further attention is given to previous publications by the early MNI group on the issue of experiential phenomena in response to electrical brain stimulation. A typical reference to Penfield’s work reads as follows: These findings were a breakthrough for 2 reasons: They demonstrated that electrical brain stimulation could artificially induce retrieval of complex memories, and they indicated that the temporal lobe played a unique role in memory because this was the main neocortical area where stimulation induced memory recall. The discovery that cortical stimulation could elicit memories prompted a number of fruitful experimental investigations. (Jacobs et al. 2012) However, as evidenced by a closer look into patients’ records and earlier reports from the MNI, it appears that this claim cannot be upheld. In reference to his own findings in patients with chronically implanted deep electrodes, the Canadian neurologist and neurophysiologist Pierre Gloor (1923–2003) from the MNI made the following statement on the characteristics of experiential phenomena: Having briefly reviewed these positive characteristics of experiential phenomena, it is important to point out that they typically also lack some features that are ordinarily part of real life experiences. Thus, the experiences do not move forward in time, with the single exception of the hallucination of hearing music. Scenes are static; they do not evolve, there is no story to be told. The patient remains passive and does not feel that he actively participates in the hallucinated scene. Perceptual detail may be fragmentary or lacking in spite of a subjective feeling of vividness of the experience. The auditory hallucination of hearing a voice is almost always without semantic content, even though the voice may sound familiar and may be identifiable. The affective tone of the voice, however, is often recognized. It is not so much cognitive detail that endows these fragmentary experiences with a sense of reality, but the feeling of “being there,” as one of our patients expressed it. (Gloor 1990) Thus, it appears questionable to what extent episodes of memory have been primarily elicited by electrical stimulation. Gloor, for example, primarily questioned the presence of any semantic content in hearing voices upon stimulation and emphasized the absence of cognitive details. Even in recent literature, experiential phenomena are confounded with human memories in complex ways, often neglecting the fragmentary nature and lack of semantic content in the phenomena elicited upon electrical stimulation. Conclusions A central point of contention in the modern neurosciences involves the specific contributions that recent neurostimulatory and neuroimaging techniques have made to the relationship between the psychophysiological sphere of the mind—as in questions of higher memory functions—and the neurobiological sphere of the brain (Gold 2009). From an interdisciplinary viewpoint on the clinical neurosciences, this development has emerged as a major discursive topic in philosophical, historical, and cultural perspectives (Stahnisch 2005). In fact, modern neuroscientific work employing electrophysiological stimulation devices and functional magnetic tomography would not have been possible without the apparatuses and instruments that embody the conceptual and research assumptions which clinical and laboratory workers apply and put to test (Stahnisch 2015). It is by no means clear, however, that what appears to hold for the clinical and physiological approaches on the one side also holds for the neurobiological approaches on the other side and vice versa (Gold 2009). The underlying assumption of neuroscientists in performing reductionist studies on memory functions to elicit the “hypothetical record of the stream of consciousness” has been characterized by Searle as a process of stimulation conversion into one common medium—the variable rates of neuron firing—leading to the explicit realization that “brains cause minds. (…) What we mean by that is that mental processes that we consider to constitute a mind are caused, entirely caused, by processes going on inside the brain” (Searle 1984). However, on closer investigation of the original historical reports by Penfield and those represented in his published articles (Penfield and Boldrey 1937; Penfield and Perot 1963; Penfield and Mathieson 1974), only a level of physical information produced by stimulation is revealed. This was then historically brought into a phenomenal context by Penfield’s clinical and research team. At the same time, it was impossible to determine any dimension of semantic content (Nitsch 2012)—such as categorizing the “percepts”—in his studies, which shows the notion of memory as a simple “process of recording” as being rather a myth in neuroscience over the past decades. In fact, detailed historical investigation shows that this notion was not backed by the fundamental patient work at the MNI at the time, yet has become so dominant in neuroscience research ever since. Moreover, work by the group around the Nobel laureates Edvard and May-Britt Moser in Norway has recently identified a “brain positioning system,” encoding physical information of space as pursued in a satellite-based “global positioning system.” Yet even this groundbreaking research has not provided any specific information as to how the neurophysiological results could practically be related to categories of meaning and intentionality. It remains astonishingly silent on the issue of “how cognition is generated in the brain” (Moser 2014). The realization of memory in solely naturalistic terms would require that modern neurology, psychiatry, and psychological memory research unequivocally demonstrates how the mental processes, which are usually interpreted as constitutive of the functioning of human mind, were exclusively caused by physiological functions in the brain itself (Moriarity et al. 2001). Taking the longer history of memory research into account, modern memory research—with increasing evidence that memory is a reconstructive function, which may include facts but also associative elements (Meade and Roediger 2009)—needs to be seen as having failed to provide the necessary mechanisms for the “neuronal encoding” as well as the “production” or “causation” of memories by stimulation of the brain. This is very much in line with recent psychiatric, pediatric, and developmental studies, for example from the Harvard Center on the Developing Child, Boston, MA, that have demonstrated problems in cognitive control, learning, and memory based on aversive workplace, school, and home contexts, which lead to persistently impaired developmental and behavioral traits (Shonkoff et al. 2009). Penfield’s original hope to arrive at an understanding of the “production” of memory with all aspects of remembrance, including his overinterpretation of the primary data (Gloor et al. 1993), as well as the selective view on H. M.'s neuropathological record and bias in his psychological tests (Dittrich 2016), exposes a strong motivation (and limitation) of the neurosciences to explain all mental phenomena in physical terms alone rather than a critical appraisal of its own data (Dossani et al. 2015). Penfield’s far-fetching claim that “the problem of neurology is to understand man himself” (Fig. 5) represents rather a conviction of an ever-recurring naturalistic research goal in the neurosciences than an evidence-based conclusion backed by his own data. Emphasizing this drawback of the naturalizing tradition in memory research does not devalue the pioneering work by Wilder Penfield and his collaborators in Montreal; however, it underscores Brenda Milner’s judgment: “they have not yet provided a sufficient clue of the underlying physiology” (Xia 2006). Figure 5. View largeDownload slide Engraved statement of Wilder Penfield displayed outside at the Montreal Neurological Institute on 3801 University Street, Montreal, Quebec, Canada. Figure 5. View largeDownload slide Engraved statement of Wilder Penfield displayed outside at the Montreal Neurological Institute on 3801 University Street, Montreal, Quebec, Canada. Funding No specific funding was provided for this research. R.N. received grants from the European Research Council (ERC-AdG “LiPsyD”) and the Deutsche Forschungsgemeinschaft (SFB 1080). Notes This work was made possible by the gratitude and openness of members of the Montreal Neurological Institute, especially Drs Richard Leblanc and Jack Antel who granted access to Penfield’s original patient records during a sabbatical of one of the authors (R.N.). The latter is especially grateful for the critical remarks and invaluable background information on the history of the MNI provided by Dr Leblanc. He gives also special thanks to the people at M.I.N.D. High School in Montreal who enabled important discussions. We also thank Dr Theodore I. Sourkes (†) at the Allan Memorial Institute, Montreal, Dr William Feindel (†), Dr Brenda Milner at the Montreal Neurological Institute, Ms Anna Dysert at the Osler Library for the History of Medicine, Dr Pascal Nicklas at the Institute of Microscopic Anatomy and Neurobiology at the Johannes Gutenberg-University Mainz, and Dr Ian Gold at McGill University in Montreal for critical discussions on the issue. We are thankful for support by Mrs Doris H. Annear, now at the Foothills Medical Centre in Calgary, the members of the History of Neuroscience Interest Group and the Mackie Family Collection in the History of Neuroscience at the University of Calgary; along with the personnel of the archives of the MNI and the AMI. We further thank Drs Brenan Smith and Cheryl Ernest for their meticulous adjustment of the English language of the article. Frank W. Stahnisch also wishes to thank Fred Weizmann (York University, Toronto) and Scott Patten (University of Calgary) for their instructive comments on earlier article versions. Conflict of Interest: none declared. References Augustinack JC , van der Kouwe AJW , Salat DH , Benner T , Stevens AA , Annese J , Fischl B , Frosch MP , Corkin S . 2014 . HM’s contributions to neuroscience: a review and autopsy studies . Hippocampus . 24 ( 11 ): 1267 – 1286 . Google Scholar CrossRef Search ADS PubMed Baldwin M 1952 . Involuntary recollections, illusions, psychical hallucinations, and emotions [MSc thesis]. [Montreal (Canada)]: McGill University. Compston A . 2005 . From the archives . Brain . 128 : 235 – 236 . Google Scholar CrossRef Search ADS PubMed Dittrich L . 2016 . Patient HM: a story of memory, madness, and family secrets . New York, NY : Random House . Dossani RH , Missios S , Nanda A . 2015 . The Legacy of Henry Molaison (1926–2008) and the impact of his bilateral mesial temporal lobe surgery on the study of human memory . World Neurosurg . 84 ( 4 ): 1127 – 1135 . Google Scholar CrossRef Search ADS PubMed Feindel W , Leblanc R . 2016 . The wounded brain healed: the golden age of the Montreal Neurological Institute, 1934–1984 . Montreal, Canada : McGill-Queen’s University Press . p. 1 – 10 . Foerster O , Penfield W . 1930 . The structural basis of traumatic epilepsy and results of radical operation . Brain . 53 ( 2 ): 99 – 119 . Google Scholar CrossRef Search ADS Gabriel M . 2017 . I am not a brain: philosophy of mind for the 21st century . New York, NY : Polity . Gavrus D . 2015 . Skill, judgement and conduct for the first generation of neurosurgeons, 1900–1930 . Medical History . 59 ( 3 ): 361 – 378 . Google Scholar CrossRef Search ADS PubMed Gloor P . 1990 . Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses . Brain . 113 ( Pt 6 ): 1673 – 1694 . Google Scholar CrossRef Search ADS PubMed Gloor P , Salanova V , Olivier A , Quesney LF . 1993 . The human dorsal hippocampal commissure. An anatomically identifiable and functional pathway . Brain . 116 ( Pt 5 ): 1249 – 1273 . Google Scholar CrossRef Search ADS PubMed Gold I . 2009 . Reduction in psychiatry . Can J Psychiatry . 54 ( 8 ): 506 – 512 . Google Scholar CrossRef Search ADS PubMed Grote M , Stadler M . 2015 . Introduction: surface histories . Sci Context . 28 ( 3 ): 311 – 315 . Google Scholar CrossRef Search ADS PubMed Guenther K . 2016 . Between clinic and experiment: Wilder Penfield’s stimulation reports and the search for mind, 1929–55 . Can Bull Med Hist . 33 ( 2 ): 281 – 320 . Google Scholar CrossRef Search ADS PubMed Hagner M . 1997 . Homo Cerebralis. Der Wandel vom Seelenorgan zum Gehirn . Berlin (Germany) : Berlin Verlag . Halgren E , Walter RD , Cherlow DG , Crandall PH . 1978 . Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala . Brain . 101 ( 1 ): 83 – 117 . Google Scholar CrossRef Search ADS PubMed Insel PS , Mattsson N , Mackin RS , Kornak J , Nosheny R , Tosun-Turgut D , Donohue MC , Aisen PS , Weiner MW . 2015 . Biomarkers and cognitive endpoints to optimize trials in Alzheimer’s disease . Ann Clin Transl Neurol . 2 ( 5 ): 534 – 547 . Google Scholar CrossRef Search ADS PubMed Jacobs J , Lega B , Anderson C . 2012 . Explaining how brain stimulation can evoke memories . J Cogn Neurosci . 24 ( 3 ): 553 – 563 . Google Scholar CrossRef Search ADS PubMed Kandel ER . 2004 . The molecular biology of memory storage: a dialog between genes and synapses . Biosci Rep . 24 ( 4–5 ): 475 – 522 . Google Scholar CrossRef Search ADS PubMed Kandel ER . 2005 . Psychiatry, psychoanalysis, and the new biology of mind . New York, NY : American Psychiatric Publishing . Kandel ER , Squire LR . 2000 . Neuroscience: breaking down scientific barriers to the study of brain and mind . Science . 290 ( 5494 ): 1113 – 1120 . Google Scholar CrossRef Search ADS PubMed Klafki HW , Staufenbiel M , Kornhuber J , Wiltfang J . 2006 . Therapeutic approaches to Alzheimer’s disease . Brain . 129 ( Pt 11 ): 2840 – 2855 . Google Scholar CrossRef Search ADS PubMed Kolb B , Teskey GC . 2012 . Age, experience, injury, and the changing brain . Dev Psychobiol . 54 ( 3 ): 311 – 325 . Google Scholar CrossRef Search ADS PubMed Loftus EF , Miller DG , Burns HJ . 1978 . Semantic integration of verbal information into a visual memory . J Exp Psychol Hum Learn . 4 ( 1 ): 19 – 31 . Google Scholar CrossRef Search ADS PubMed Meade ML , Roediger HL . 2009 . Age differences in collaborative memory: the role of retrieval manipulations . Mem Cognit . 37 ( 7 ): 962 – 975 . Google Scholar CrossRef Search ADS PubMed Millett D . 2001 . Hans Berger: from psychic energy to the EEG . Perspect Biol Med . 44 ( 4 ): 522 – 542 . Google Scholar CrossRef Search ADS PubMed Milner B . 1977 . Wilder Penfield: his legacy to neurology. Memory mechanisms . Can Med Assoc J . 116 ( 12 ): 1374 – 1376 . Google Scholar PubMed Milner B , Klein D . 2016 . Loss of recent memory after bilateral hippocampal lesions: memory and memories-looking back and looking forward . J Neurol Neurosurg Psychiatry . 87 ( 3 ): 230 . Google Scholar CrossRef Search ADS PubMed Milner B , Squire LR , Kandel ER . 1998 . Cognitive neuroscience and the study of memory . Neuron . 20 ( 3 ): 445 – 468 . Google Scholar CrossRef Search ADS PubMed Moriarity JL , Boatman D , Krauss GL , Storm PB , Lenz FA . 2001 . Human “memories” can be evoked by stimulation of the lateral temporal cortex after ipsilateral medial temporal lobe resection . J Neurol Neurosurg Psychiatry . 71 ( 4 ): 549 – 551 . Google Scholar CrossRef Search ADS PubMed Moser E . Facts Nobelprize.org. 2014 . Stockholm (Sweden): Nobel Media AB [accessed on 2018 February 5]. http://www.nobelprize.org/nobel_prizes/medicine/laureates/2014/edvard-moser-facts.html Nitsch R . 2012 . Gehirn, Geist und Bedeutung: Zur Stellung der Neurowissenschaften in der Leib-Seele-Diskussion . Münster (Germany) : Mentis . p. 17 . O’Keefe J , Nadel L . 1978 . The Hippocampus as a Cognitive Map . Oxford (England) : Oxford University Press . p. 410 . Penfield W . 1938 . The cerebral cortex in man: I. The cerebral cortex and consciousness . Arch Neurol Psychiatry . 40 ( 3 ): 417 – 442 . Google Scholar CrossRef Search ADS Penfield W . 1950 . Gordon Wilson lecture, the mechanism of memory . Trans Am Clin Climatol Assoc . 62 : 165 – 169 . Google Scholar PubMed Penfield W , Boldrey E . 1937 . Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation . Brain . 60 ( 4 ): 389 – 443 . Google Scholar CrossRef Search ADS Penfield W , Mathieson G . 1974 . Memory. Autopsy findings and comments on the role of hippocampus in experiential recall . Arch Neurol . 31 ( 3 ): 145 – 154 . Google Scholar CrossRef Search ADS PubMed Penfield W , Perot P . 1963 . The brain’s record of auditory and visual experience . Brain . 86 : 595 – 696 . Google Scholar CrossRef Search ADS PubMed Penfield W , Rasmussen T . 1950 . The cerebral cortex of man . New York, NY : Macmillan Company . Roediger HL , DeSoto KA . 2015 . The psychology of reconstructive memory. In: Wright J , editor . International encyclopedia of the social & behavioral sciences . 2nd ed . Oxford, United Kingdom : Elsevier . p. 50 – 55 . Scoville WB , Milner B . 1957 . Loss of recent memory after bilateral hippocampal lesions . J Neurol Neurosurg Psychiatry . 20 ( 1 ): 11 – 21 . Google Scholar CrossRef Search ADS PubMed Searle JR . 1984 . Minds, brains and science . Cambridge, MA : Harvard University Press . Searle JR . 1992 . The rediscovery of the mind . Cambridge, MA : MIT Press . Shonkoff JP , Boyce WT , McEwen BS . 2009 . Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention . J Am Med Assoc . 301 ( 21 ): 2252 – 2259 . Google Scholar CrossRef Search ADS Snyder PJ , Whitaker HA . 2013 . Neurologic heuristics and artistic whimsy: the cerebral cartography of Wilder Penfield . J Hist Neurosci . 22 ( 3 ): 277 – 291 . Google Scholar CrossRef Search ADS PubMed Squire LR . 2009 . Memory and brain systems: 1969–2009 . J Neurosci . 29 ( 41 ): 12711 – 12716 . Google Scholar CrossRef Search ADS PubMed Stahnisch FW . 2005 . Historical and philosophical perspectives on experimental practice in medicine and the life sciences . Theor Med Bioeth . 26 ( 5 ): 397 – 425 . Google Scholar CrossRef Search ADS PubMed Stahnisch FW . 2008 . Zur Zwangsemigration deutschsprachiger Neurowissenschaftler nach Nordamerika. Der historische Fall des Montreal Neurological Institute. In: Keil G , Holdorff B , editors . Schriftenreihe der Deutschen Gesellschaft für Geschichte der Nervenheilkunde . Würzburg, Germany : Königshausen und Neumann . p. 414 – 442 . Stahnisch FW . 2015 . Nonrestraint, shock therapies, and brain stimulation approaches: patient autonomy and the emergence of modern neuropsychiatry. In: Clausen J , Levy N , editors . Handbook of neuroethics . Dordrecht, Netherlands : Springer . p. 519 – 533 . Xia C . 2006 . Understanding the human brain: a lifetime of dedicated pursuit. Interview with Dr. Brenda Milner . McGill J Med . 9 ( 2 ): 165 – 172 . Google Scholar PubMed © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
TI - Neuronal Mechanisms Recording the Stream of Consciousness–A Reappraisal of Wilder Penfield’s (1891–1976) Concept of Experiential Phenomena Elicited by Electrical Stimulation of the Human Cortex
JF - Cerebral Cortex
DO - 10.1093/cercor/bhy085
DA - 2018-09-01
UR - https://www.deepdyve.com/lp/oxford-university-press/neuronal-mechanisms-recording-the-stream-of-consciousness-a-jmFXXyK0fB
SP - 3347
EP - 3355
VL - 28
IS - 9
DP - DeepDyve
ER -