- Email: [email protected]
Epilepsy and brain function: Common ideas of Hughlings-Jackson and Wilder Penfield
Epilepsy & Behavior 24 (2012) 311–313
Contents lists available at SciVerse ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Review
Epilepsy and brain function: Common ideas of Hughlings-Jackson and Wilder Penfield R. Edward Hogan ⁎, Edward A. English Washington University in St. Louis, USA
a r t i c l e
i n f o
Article history: Received 8 March 2012 Revised 9 April 2012 Accepted 21 April 2012 Available online 30 May 2012 Keywords: Epilepsy Epilepsy surgery Temporal lobe epilepsy Consciousness History Déjà vu
a b s t r a c t From studies of epilepsy, Hughlings-Jackson proposed a model of brain function including levels of consciousness, a hierarchy of nervous centers, and a sensory–motor relationship. Hughlings-Jackson's ideas influenced Wilder Penfield, a pioneer of electrical stimulation for mapping of the human cerebral cortex. From his work with electrocortical stimulation in patients with epilepsy, Penfield observed what he referred to as a “record of the stream of consciousness,” similar to Hughlings-Jackson's “subject consciousness.” Penfield expanded upon Hughlings-Jackson's work and suggested that although higher and lower centers explained reflex movements, another separate unaccounted for force controlled voluntary movements. These two functional units he termed the “computer (or automatic sensory–motor mechanism)” and the “mind's mechanism (or highest brain mechanism).” The ideas of John Hughlings-Jackson and Wilder Penfield represent a continuum of thought about the relationship of epilepsy and brain function and continue to be relevant to our current understanding of memory function and the mind–brain relationship. © 2012 Elsevier Inc. All rights reserved.
1. Introduction John Hughlings-Jackson and Wilder Penfield both made enduring contributions to the understanding of epilepsy and brain function. Before the advent of modern neurological technologies such as electroencephalography or neuroimaging, Hughlings-Jackson used years of observing patients and his keen clinical reasoning skills to develop a revolutionary model of brain function and organization. Drawing from his clinical observations in patients with neurological disease and experience working with patients with epilepsy, HughlingsJackson laid a foundation of ideas that changed the way others saw the brain and consciousness [1]. According to Hughlings-Jackson, watching the effects of epilepsy played a crucial role in his ability to understand the workings of the brain, as he claims. “No better neurological work can be done than the precise investigation of epileptic paroxysms” [2]. Hughlings-Jackson's model of brain function and organization included ideas about levels of consciousness, a hierarchy of nervous centers, and a sensory–motor relationship [3] that would later influence the work of prominent psychologists, philosophers, neurologists, and neurosurgeons. In particular, Hughlings-Jackson's ideas enabled the prominent neurosurgeon Wilder Penfield to establish new ideas about stored consciousness of the brain and the function of the mind. Few efforts have been made to trace Hughlings-Jackson's influence on Penfield; ⁎ Corresponding author at: Washington University in St. Louis, Campus Box 8111, 660 S. Euclid Ave., St. Louis, MO 63110, USA. Fax: + 1 314 362 0296. E-mail address: [email protected] (R.E. Hogan). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.04.124
yet examining how Penfield formed his innovative ideas from Hughlings-Jackson's work reveals the enduring legacies that both Hughlings-Jackson and Penfield continue to have in the world of psychology, philosophy, and neuroscience. 2. Hughlings-Jackson's concepts of consciousness John Hughlings-Jackson was known for his philosophic disposition and indeed considered abandoning the practice of medicine altogether and taking up philosophy [4–7]. Integrating his philosophical ideas with his observations of neurological disease and epilepsy [7–9], Hughlings-Jackson formulated concepts of consciousness and a model of brain function based on a hierarchy of nervous centers [10]. The lowest hierarchical nervous centers were represented at the spinal cord and peripheral nerve levels while the highest hierarchical nervous centers were represented in the cerebral cortex. Hughlings-Jackson believed that the nervous system evolved into a pyramid of ever increasing complexity, heterogeneity, and flexibility. The lower centers being more rigid, less specialized, and automatic (primarily representing autonomic function) and the higher centers being more flexible, more specialized, and voluntary (primarily representing higher cognitive function) [11,12]. In addition to his hierarchical model of brain function, HughlingsJackson incorporated ideas of sensory–motor function in the brain with his levels of nervous function and consciousness. He proposed the deep tendon reflex, with its initial sensory and subsequent motor components, as a simple, lower level reflex representing sensory– motor function [13]. He extended this idea of simple sensory–motor
312
R.E. Hogan, E.A. English / Epilepsy & Behavior 24 (2012) 311–313
function at lower centers to also apply to higher centers but in a much more complex relationship [3]. At higher centers, because of the greater complexity of representation of sensory and motor components, he entitled the concept “sensori-motor.” From the sensori-motor concept, Hughlings-Jackson proposed two “halves” of brain function. One half represented the sensory or “subjective” half of brain function while the other half represented the motor or “objective” half of brain function [14]. He proposed an example of the representations of interaction of subjective and objective components of brain function in complex partial seizures involving a feeling of familiarity, a phenomenon which Hughlings-Jackson called “dreamy state” [2] but is more often referred to as déjà vu in contemporary literature. Patients state positive symptoms of “knowing” or “recollection” (a representation of an increase in subjective component function) but have an associated deficit of consciousness which often results in an inability to remember the idea associated with “knowing the subject associated with ‘recollection’” (a representation of a decrease in objective component function). From the concept of subjective and objective brain function, HughlingsJackson proposed the ideas of subject and object consciousness [12]. To describe subject consciousness, he used the example of sensory representations when visualizing an object [12]. The object is initially perceived at all sensory levels. This produced a sensory representation of the object. The next day, one can think of the object and have a mental idea of it, without actually seeing the object. This mental representation is the sensory or subject consciousness for the object, based on the stored information of the initial perception of it. Stated another way, subject consciousness represents our stored memories. What enables one to think of the object? This is the other half of consciousness, the motor side of consciousness, which HughlingsJackson termed “object consciousness.” Object consciousness is the faculty of “calling up” mental images into consciousness, the mental ability to direct attention to aspects of subject consciousness [13]. 3. Wilder Penfield's outline of brain function Hughlings-Jackson's ideas of a hierarchy of nervous centers and his thoughts on consciousness and sensory–motor function later played a significant role in the theories of Wilder Penfield. As a neurosurgeon, Penfield performed pioneering work with electrode stimulation of the brain, thereby mapping the human cerebral cortex. Penfield openly credited Hughlings-Jackson as an inspiration for his ideas. Penfield dedicated his classic textbook “Epilepsy and the Functional Anatomy of the Human Brain” [15] to Hughlings-Jackson. Penfield's comments about Hughlings-Jackson's influence in the field of neurology were as follows: “Jackson came to be London's great prophet of neurology because he read the meanings of epilepsy in terms of brain function. He surmised the truth, that in each epileptic seizure there is a discharge, a release of energy, in gray matter of the brain. He saw the result, in each case, as in illuminating experiment that could throw light on the functional ‘arrangements’ within the brain.” [16,17]. The parallels of the interest of Hughlings-Jackson and Penfield are obvious, in that both were interested in understanding brain function through observations in patients with epileptic seizures. Penfield, however, had the advantage of improvements in neuro-diagnostic tools, such as the electroencephalogram, as well as experience in the surgical treatment of epilepsy, which he included his groundbreaking experiments in direct electrocortical stimulation of the human brain. Penfield states that his early interest in the mind–brain relationship began during his study in decerebrate cats in the 1920s. He carried these early interests with him as he progressed in his career, including his pioneering work in the surgical treatment of epilepsy
within the Montréal Neurological Institute [18–20]. Early in his experience with direct electrocortical stimulation of the brain, Penfield found that electrical activation of the lateral temporal region sometimes evoked a “sequential record of consciousness, a record that had been laid down during the patient's earlier experience. The patient ‘relived’ all that he had been aware of in that earlier period of time as in a moving-picture ‘flashback.’” Penfield made the association of this phenomenon with Hughlings-Jackson's description of “dreamy states” or “psychical seizures” [21,22] and recognized that the associated symptoms of “stream of consciousness” elicited by electrocortical stimulation and by epileptic seizures reflected a similar neurophysiological phenomenon. Additionally, Penfield made the observation that despite experiencing a “flashback” of previous memories and situations during electrocortical stimulation, patients were also aware of their current surroundings and could relate the phenomenon in the context of being in the operating room and reporting the experience to him. He therefore made conclusions that past memories of perceived phenomena were preserved under one mechanism, which could be discriminated from phenomena currently perceived, which were therefore stored and interpreted by a separate mechanism. Penfield states “many a patient has told me that the experience brought back by the electrode is much more real than remembering. And yet he is still aware of the present situation. There is a doubling of consciousness, and yet he knows which is the present” [21,23]. He concludes that there is “hidden away in the brain, a record of the stream of consciousness. It seems to hold the detail of that stream as laid down during each man's waking conscious hours.” Building on his idea of the “doubling of consciousness” phenomenon, Penfield suggested that while higher and lower centers explained reflex movements, another unaccounted for force controlled voluntary movements. He proposed two functional units, the “computer (or automatic sensory–motor mechanism)” and the “mind's mechanism (or highest brain mechanism)”, respectively, for reflex and voluntary actions. He proposed that a region of the brain, defined as cortex which when electrically stimulated resulted in evoking past memories and experiential phenomenon, played a critical role for interpretation between the two functional units. He therefore labeled this cortex the “interpretive cortex,” proposing its localization in an area of cortex that “covers most of the superior surfaces of the temporal lobes, as well as the lateral and probably the inferior surfaces” [24,25]. At the end of his career, Penfield authored a book entitled “The Mystery of the Mind” [16]. In this volume, Penfield integrates his lifelong experience in treating patients with epileptic seizures to formulate ideas about the mind–brain relationship. He integrates many of the interests of Hughlings-Jackson with his presentation of epileptic seizures as a guide to understand brain function and the mind. Penfield's integration of observations and critiques of the book “Mystery of the Mind” from neurologist Sir Charles Simmons and philosopher Charles Hendell also parallels the interests of the neurologist/ philosopher Hughlings-Jackson. 4. Contemporary findings Hughlings-Jackson's “subject consciousness” and Penfield's “record of the stream of consciousness” are interestingly similar. Both propose conceptual frameworks for storage of past memories. Based in part on Hughlings-Jackson's earlier work, Penfield further added ideas about localization and interpretation of stored memories [25,26]. Further investigation of both Hughlings-Jackson's and Penfield's ideas have led to better clarification of their ideas and have provided a framework for interpretation of new findings in brain function. For example, further investigation into the localization of brain regions related to functions of Penfield's “interpretive cortex” has shown that stimulation of either the temporal neocortex, anterior hippocampus, or amygdala
R.E. Hogan, E.A. English / Epilepsy & Behavior 24 (2012) 311–313
could evoke such symptoms [27]. Proportionally, the hippocampus and amygdala were more likely the lateral neocortical structures to evoke the “dreamy state” and associated experiential symptoms. Due to the technical limitations of his time, Penfield was unable to routinely include mesial temporal structures in his stimulation studies, which likely explains his emphasis on temporal neocortical structures as “interpretive cortex.” Past investigators have approached the relationship of epilepsy and consciousness from different perspectives. Hughlings-Jackson's and Penfield's approach, using the phenomenology of electrocorticography and epilepsy to define a system of mind and consciousness, differs from the approach of other investigators. In a review of the concept of consciousness in epilepsy, Gloor [28] drew on epistemological and scientific arguments to attempt to define consciousness, which he admits may never be possible, to illustrate that such definitions provide little to further the understanding of epilepsy. However, he proposed that aspects of conscious experience such as perception, cognition, memory, affect, and voluntary motility were open to neurobiological research. While such an approach adequately outlines the complexity of consciousness, it emphasizes study of separate aspects of epilepsy, rather than more global processes underlying epilepsy, to relate changes in consciousness to epileptic phenomena. Contrasting this approach is that of Hughlings-Jackson and Penfield, who circumvented many of the difficulties in defining consciousness by using changes induced by epileptic seizures to define it [11]. Further interesting contemporary insights, related to the ideas of memory function, continue from investigation of patients with epilepsy with electrocorticography, adding further information about Penfield's idea of “interpretive cortex.” Quiroga et al. [29], using depth electrodes in combination with micro-wires, analyzed responses of neurons from the hippocampus, amygdala, entorhinal cortex, and parahippocampal gyrus to different images. They report on a subset of mesial temporal neurons that are selectively activated by strikingly different pictures of given individuals, landmarks, or objects. In some cases, activation occurred by letter representations of their names. For example, one subject in the study showed activation of a single unit in the right anterior hippocampus when viewing pictures of the actress Halle Berry but not when viewing images of other individuals. Interestingly, the letter string “Halle Berry” also selectively activated the unit. This suggests that neurons encode an abstract representation of an individual. These results provide insight into complex visual perception and its integration into longterm and more abstract memories. In summary, the ideas of John Hughlings-Jackson and Wilder Penfield represent a continuum of thought about the relationship of epilepsy and brain function. Hughlings-Jackson proposed a framework for brain function and consciousness, upon which Penfield expanded with information obtained primarily from electrocorticographical stimulation studies of subjects under evaluation for epilepsy surgery. Their ideas continue to be relevant to our current understanding of memory function and the mind–brain relationship.
313
References [1] York III GK, Steinberg DA. Hughlings Jackson's neurological ideas. Brain 2011;134: 3106–13. [2] Hughlings-Jackson J. On a particular variety of epilepsy (“intellectual aura”), one case with symptoms of organic brain disease. Brain 1888;11:179–207. [3] Hughlings-Jackson J. Evolution and dissolution of the nervous system (Croonian Lectures). In: Taylor J, editor. The selected writings of John Hughlings Jackson. New York: Basic Books, Inc.; 1958. p. 45–75. [4] Temkin O. The end of the falling sickness? The falling sickness. A history of epilepsy from the Greeks to the beginning of modern neurology. Baltimore: The Johns Hopkins University Press; 1971. p. 347–82. [5] Critchley M, Critchley EA. John Hughlings Jackson: father of English neurology. New York: Oxford University Press; 1998. p. 1–228. [6] York GK, Steinberg DA. The philosophy of Hughlings Jackson. J R Soc Med 2002;95:314–8. [7] York GK, Steinberg DA. An introduction to the life and work of John Hughlings Jackson with a catalogue raisonne of his writings. Med Hist 2006:3–157 [Suppl.]. [8] Hughlings-Jackson J. On temporary mental disorders after epileptic paroxysms. In: Talyor J, editor. The selected writings of John Hughlings Jackson. New York: Basic Books, Inc.; 1958. p. 119–34. [9] Hughlings-Jackson J. Remarks on systemic sensations in epilepsies. In: Taylor J, editor. Selected writings of John Hughlings Jackson. New York: Basic Books, Inc.; 1958. p. 118. [10] Steinberg DA, York GK. Hughlings Jackson, concomitance, and mental evolution. J Hist Neurosci 1994;3:169–76. [11] Hogan RE, Kaiboriboon K. The “dreamy state”: John Hughlings-Jackson's ideas of epilepsy and consciousness. Am J Psychiatry 2003;160:1740–7. [12] Hughlings-Jackson J. Remarks on dissolution of the nervous system as exemplified by certain post-epileptic conditions. In: Taylor J, editor. The selected writings of John Hughlings Jackson. New York: Basic Books, Inc.; 1958. p. 3–28. [13] Hughlings-Jackson J. On the scientific and empirical investigation of epilepsies. In: Taylor J, editor. The selected writings of John Hughlings Jackson. New York: Basic Books, Inc.; 1958. p. 162–273. [14] Hughlings-Jackson J. On right- or left-sided spasm at the onset of epileptic paroxysms and on crude sensation warnings and elaborate mental states. In: Taylor J, editor. The selected writings of John Hughlings Jackson. New York: Basic Books, Inc.; 1958. p. 308–17. [15] Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown and Co.; 1954. [16] Penfield W. The mystery of the mind: a critical study of consciousness and the human brain. Princeton, New Jersey: Princeton University Press; 1975. [17] Penfield W. Afterthoughts by the author. The mystery of the mind. Princeton, New Jersey: Princeton University Press; 1975. p. 102–15. [18] Lewis J. Something hidden: a biography of Wilder Penfield. Toronto: Doubleday & Company, Inc.; 1981. [19] Penfield W. No man alone: a neurosurgeon's life. Boston: Little, Brown and Company; 1977. [20] Penfield W. The cerebral cortex in man: the cerebral cortex and consciousness. Arch Neurol Psychiatry 1930;40:417–22. [21] Penfield W. The stream of consciousness electrically reactivated. The mystery of the mind. Princeton, New Jersey: Princeton University Press; 1975. p. 21–7. [22] Penfield W. Sherringtonian alternatives—two fundamental elements or only one? The mystery of the mind. Princeton, New Jersey: Princeton University Press; 1975. p. 3–6. [23] Penfield W. Some mechanisms of consciousness discovered during electrical stimulation of the brain. Proc Natl Acad Sci U S A 1958;44:51–66. [24] Penfield W. The interpretive cortex; the stream of consciousness in the human brain can be electrically reactivated. Science 1959;129:1719–25. [25] Penfield W. The indispensable substratum of consciousness. The mystery of the mind. Princeton, New Jersey: Princeton University Press; 1975. p. 18–20. [26] Penfield W. The excitable cortex in conscious man. [The 5th Sherrington Lecture]. Liverpool University Press; 1958. [27] Bancaud J, Brunet-Bourgin F, Chauvel P, Halgren E. Anatomical origin of deja vu and vivid ‘memories’ in human temporal lobe epilepsy. Brain 1994;117:71–90. [28] Gloor P. Consciousness as a neurological concept in epileptology: a critical review. Epilepsia 1986;27(Suppl. 2):S14–26. [29] Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. Invariant visual representation by single neurons in the human brain. Nature 2005;435:1102–7.
Contents lists available at SciVerse ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Review
Epilepsy and brain function: Common ideas of Hughlings-Jackson and Wilder Penfield R. Edward Hogan ⁎, Edward A. English Washington University in St. Louis, USA
a r t i c l e
i n f o
Article history: Received 8 March 2012 Revised 9 April 2012 Accepted 21 April 2012 Available online 30 May 2012 Keywords: Epilepsy Epilepsy surgery Temporal lobe epilepsy Consciousness History Déjà vu
a b s t r a c t From studies of epilepsy, Hughlings-Jackson proposed a model of brain function including levels of consciousness, a hierarchy of nervous centers, and a sensory–motor relationship. Hughlings-Jackson's ideas influenced Wilder Penfield, a pioneer of electrical stimulation for mapping of the human cerebral cortex. From his work with electrocortical stimulation in patients with epilepsy, Penfield observed what he referred to as a “record of the stream of consciousness,” similar to Hughlings-Jackson's “subject consciousness.” Penfield expanded upon Hughlings-Jackson's work and suggested that although higher and lower centers explained reflex movements, another separate unaccounted for force controlled voluntary movements. These two functional units he termed the “computer (or automatic sensory–motor mechanism)” and the “mind's mechanism (or highest brain mechanism).” The ideas of John Hughlings-Jackson and Wilder Penfield represent a continuum of thought about the relationship of epilepsy and brain function and continue to be relevant to our current understanding of memory function and the mind–brain relationship. © 2012 Elsevier Inc. All rights reserved.
1. Introduction John Hughlings-Jackson and Wilder Penfield both made enduring contributions to the understanding of epilepsy and brain function. Before the advent of modern neurological technologies such as electroencephalography or neuroimaging, Hughlings-Jackson used years of observing patients and his keen clinical reasoning skills to develop a revolutionary model of brain function and organization. Drawing from his clinical observations in patients with neurological disease and experience working with patients with epilepsy, HughlingsJackson laid a foundation of ideas that changed the way others saw the brain and consciousness [1]. According to Hughlings-Jackson, watching the effects of epilepsy played a crucial role in his ability to understand the workings of the brain, as he claims. “No better neurological work can be done than the precise investigation of epileptic paroxysms” [2]. Hughlings-Jackson's model of brain function and organization included ideas about levels of consciousness, a hierarchy of nervous centers, and a sensory–motor relationship [3] that would later influence the work of prominent psychologists, philosophers, neurologists, and neurosurgeons. In particular, Hughlings-Jackson's ideas enabled the prominent neurosurgeon Wilder Penfield to establish new ideas about stored consciousness of the brain and the function of the mind. Few efforts have been made to trace Hughlings-Jackson's influence on Penfield; ⁎ Corresponding author at: Washington University in St. Louis, Campus Box 8111, 660 S. Euclid Ave., St. Louis, MO 63110, USA. Fax: + 1 314 362 0296. E-mail address: [email protected] (R.E. Hogan). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.04.124
yet examining how Penfield formed his innovative ideas from Hughlings-Jackson's work reveals the enduring legacies that both Hughlings-Jackson and Penfield continue to have in the world of psychology, philosophy, and neuroscience. 2. Hughlings-Jackson's concepts of consciousness John Hughlings-Jackson was known for his philosophic disposition and indeed considered abandoning the practice of medicine altogether and taking up philosophy [4–7]. Integrating his philosophical ideas with his observations of neurological disease and epilepsy [7–9], Hughlings-Jackson formulated concepts of consciousness and a model of brain function based on a hierarchy of nervous centers [10]. The lowest hierarchical nervous centers were represented at the spinal cord and peripheral nerve levels while the highest hierarchical nervous centers were represented in the cerebral cortex. Hughlings-Jackson believed that the nervous system evolved into a pyramid of ever increasing complexity, heterogeneity, and flexibility. The lower centers being more rigid, less specialized, and automatic (primarily representing autonomic function) and the higher centers being more flexible, more specialized, and voluntary (primarily representing higher cognitive function) [11,12]. In addition to his hierarchical model of brain function, HughlingsJackson incorporated ideas of sensory–motor function in the brain with his levels of nervous function and consciousness. He proposed the deep tendon reflex, with its initial sensory and subsequent motor components, as a simple, lower level reflex representing sensory– motor function [13]. He extended this idea of simple sensory–motor
312
R.E. Hogan, E.A. English / Epilepsy & Behavior 24 (2012) 311–313
function at lower centers to also apply to higher centers but in a much more complex relationship [3]. At higher centers, because of the greater complexity of representation of sensory and motor components, he entitled the concept “sensori-motor.” From the sensori-motor concept, Hughlings-Jackson proposed two “halves” of brain function. One half represented the sensory or “subjective” half of brain function while the other half represented the motor or “objective” half of brain function [14]. He proposed an example of the representations of interaction of subjective and objective components of brain function in complex partial seizures involving a feeling of familiarity, a phenomenon which Hughlings-Jackson called “dreamy state” [2] but is more often referred to as déjà vu in contemporary literature. Patients state positive symptoms of “knowing” or “recollection” (a representation of an increase in subjective component function) but have an associated deficit of consciousness which often results in an inability to remember the idea associated with “knowing the subject associated with ‘recollection’” (a representation of a decrease in objective component function). From the concept of subjective and objective brain function, HughlingsJackson proposed the ideas of subject and object consciousness [12]. To describe subject consciousness, he used the example of sensory representations when visualizing an object [12]. The object is initially perceived at all sensory levels. This produced a sensory representation of the object. The next day, one can think of the object and have a mental idea of it, without actually seeing the object. This mental representation is the sensory or subject consciousness for the object, based on the stored information of the initial perception of it. Stated another way, subject consciousness represents our stored memories. What enables one to think of the object? This is the other half of consciousness, the motor side of consciousness, which HughlingsJackson termed “object consciousness.” Object consciousness is the faculty of “calling up” mental images into consciousness, the mental ability to direct attention to aspects of subject consciousness [13]. 3. Wilder Penfield's outline of brain function Hughlings-Jackson's ideas of a hierarchy of nervous centers and his thoughts on consciousness and sensory–motor function later played a significant role in the theories of Wilder Penfield. As a neurosurgeon, Penfield performed pioneering work with electrode stimulation of the brain, thereby mapping the human cerebral cortex. Penfield openly credited Hughlings-Jackson as an inspiration for his ideas. Penfield dedicated his classic textbook “Epilepsy and the Functional Anatomy of the Human Brain” [15] to Hughlings-Jackson. Penfield's comments about Hughlings-Jackson's influence in the field of neurology were as follows: “Jackson came to be London's great prophet of neurology because he read the meanings of epilepsy in terms of brain function. He surmised the truth, that in each epileptic seizure there is a discharge, a release of energy, in gray matter of the brain. He saw the result, in each case, as in illuminating experiment that could throw light on the functional ‘arrangements’ within the brain.” [16,17]. The parallels of the interest of Hughlings-Jackson and Penfield are obvious, in that both were interested in understanding brain function through observations in patients with epileptic seizures. Penfield, however, had the advantage of improvements in neuro-diagnostic tools, such as the electroencephalogram, as well as experience in the surgical treatment of epilepsy, which he included his groundbreaking experiments in direct electrocortical stimulation of the human brain. Penfield states that his early interest in the mind–brain relationship began during his study in decerebrate cats in the 1920s. He carried these early interests with him as he progressed in his career, including his pioneering work in the surgical treatment of epilepsy
within the Montréal Neurological Institute [18–20]. Early in his experience with direct electrocortical stimulation of the brain, Penfield found that electrical activation of the lateral temporal region sometimes evoked a “sequential record of consciousness, a record that had been laid down during the patient's earlier experience. The patient ‘relived’ all that he had been aware of in that earlier period of time as in a moving-picture ‘flashback.’” Penfield made the association of this phenomenon with Hughlings-Jackson's description of “dreamy states” or “psychical seizures” [21,22] and recognized that the associated symptoms of “stream of consciousness” elicited by electrocortical stimulation and by epileptic seizures reflected a similar neurophysiological phenomenon. Additionally, Penfield made the observation that despite experiencing a “flashback” of previous memories and situations during electrocortical stimulation, patients were also aware of their current surroundings and could relate the phenomenon in the context of being in the operating room and reporting the experience to him. He therefore made conclusions that past memories of perceived phenomena were preserved under one mechanism, which could be discriminated from phenomena currently perceived, which were therefore stored and interpreted by a separate mechanism. Penfield states “many a patient has told me that the experience brought back by the electrode is much more real than remembering. And yet he is still aware of the present situation. There is a doubling of consciousness, and yet he knows which is the present” [21,23]. He concludes that there is “hidden away in the brain, a record of the stream of consciousness. It seems to hold the detail of that stream as laid down during each man's waking conscious hours.” Building on his idea of the “doubling of consciousness” phenomenon, Penfield suggested that while higher and lower centers explained reflex movements, another unaccounted for force controlled voluntary movements. He proposed two functional units, the “computer (or automatic sensory–motor mechanism)” and the “mind's mechanism (or highest brain mechanism)”, respectively, for reflex and voluntary actions. He proposed that a region of the brain, defined as cortex which when electrically stimulated resulted in evoking past memories and experiential phenomenon, played a critical role for interpretation between the two functional units. He therefore labeled this cortex the “interpretive cortex,” proposing its localization in an area of cortex that “covers most of the superior surfaces of the temporal lobes, as well as the lateral and probably the inferior surfaces” [24,25]. At the end of his career, Penfield authored a book entitled “The Mystery of the Mind” [16]. In this volume, Penfield integrates his lifelong experience in treating patients with epileptic seizures to formulate ideas about the mind–brain relationship. He integrates many of the interests of Hughlings-Jackson with his presentation of epileptic seizures as a guide to understand brain function and the mind. Penfield's integration of observations and critiques of the book “Mystery of the Mind” from neurologist Sir Charles Simmons and philosopher Charles Hendell also parallels the interests of the neurologist/ philosopher Hughlings-Jackson. 4. Contemporary findings Hughlings-Jackson's “subject consciousness” and Penfield's “record of the stream of consciousness” are interestingly similar. Both propose conceptual frameworks for storage of past memories. Based in part on Hughlings-Jackson's earlier work, Penfield further added ideas about localization and interpretation of stored memories [25,26]. Further investigation of both Hughlings-Jackson's and Penfield's ideas have led to better clarification of their ideas and have provided a framework for interpretation of new findings in brain function. For example, further investigation into the localization of brain regions related to functions of Penfield's “interpretive cortex” has shown that stimulation of either the temporal neocortex, anterior hippocampus, or amygdala
R.E. Hogan, E.A. English / Epilepsy & Behavior 24 (2012) 311–313
could evoke such symptoms [27]. Proportionally, the hippocampus and amygdala were more likely the lateral neocortical structures to evoke the “dreamy state” and associated experiential symptoms. Due to the technical limitations of his time, Penfield was unable to routinely include mesial temporal structures in his stimulation studies, which likely explains his emphasis on temporal neocortical structures as “interpretive cortex.” Past investigators have approached the relationship of epilepsy and consciousness from different perspectives. Hughlings-Jackson's and Penfield's approach, using the phenomenology of electrocorticography and epilepsy to define a system of mind and consciousness, differs from the approach of other investigators. In a review of the concept of consciousness in epilepsy, Gloor [28] drew on epistemological and scientific arguments to attempt to define consciousness, which he admits may never be possible, to illustrate that such definitions provide little to further the understanding of epilepsy. However, he proposed that aspects of conscious experience such as perception, cognition, memory, affect, and voluntary motility were open to neurobiological research. While such an approach adequately outlines the complexity of consciousness, it emphasizes study of separate aspects of epilepsy, rather than more global processes underlying epilepsy, to relate changes in consciousness to epileptic phenomena. Contrasting this approach is that of Hughlings-Jackson and Penfield, who circumvented many of the difficulties in defining consciousness by using changes induced by epileptic seizures to define it [11]. Further interesting contemporary insights, related to the ideas of memory function, continue from investigation of patients with epilepsy with electrocorticography, adding further information about Penfield's idea of “interpretive cortex.” Quiroga et al. [29], using depth electrodes in combination with micro-wires, analyzed responses of neurons from the hippocampus, amygdala, entorhinal cortex, and parahippocampal gyrus to different images. They report on a subset of mesial temporal neurons that are selectively activated by strikingly different pictures of given individuals, landmarks, or objects. In some cases, activation occurred by letter representations of their names. For example, one subject in the study showed activation of a single unit in the right anterior hippocampus when viewing pictures of the actress Halle Berry but not when viewing images of other individuals. Interestingly, the letter string “Halle Berry” also selectively activated the unit. This suggests that neurons encode an abstract representation of an individual. These results provide insight into complex visual perception and its integration into longterm and more abstract memories. In summary, the ideas of John Hughlings-Jackson and Wilder Penfield represent a continuum of thought about the relationship of epilepsy and brain function. Hughlings-Jackson proposed a framework for brain function and consciousness, upon which Penfield expanded with information obtained primarily from electrocorticographical stimulation studies of subjects under evaluation for epilepsy surgery. Their ideas continue to be relevant to our current understanding of memory function and the mind–brain relationship.
313
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