Robert A Novelly. American Psychologist. Volume 47, Issue 9, September 1992.
Both neuropsychology and psychology in general have been enhanced markedly by brain-behavior models derived from the study of the epilepsies. A significant body of neuropsychological concepts originated or were confirmed through epilepsy-based treatment and research. These concepts include the peri-Rolandic homunculus, the role of the hippocampal-temporal lobe complex in cognitive memory, hemisphere plasticity for speech in childhood, the intracarotid amytal procedure for determining hemisphere memory patency, and hemisphere-based models of cognition confirmed through human commissurotomy. Personality and social-emotional research in epilepsy are additional areas in which new conceptual models grounded in psychological science can both repay our debt to the epilepsies and provide much needed psychological research and treatment.
When you read an article, undertake a study program, or diagnose patients incorporating clinical neuropsychological concepts, there is a substantial probability that you are learning or using fundamental concepts derived from the scientifically bountiful field of the epilepsies. The Greek origin of the term epilepsy, “grabbed hold of from above” (epi = from above, leptos = to grab hold of), denotes the dramatic symptoms of a generalized tonic-clonic epileptic seizure. In fact, the epilepsies are a spectrum of episodic behavioral symptoms arising from numerous and different neuronal abnormalities and are associated with a pathognomonic electroencephalogram (EEG). With the possible exception of cerebral stroke, which has provided insights into aphasic and hemineglect syndromes, no other cerebral (central nervous system; CNS) disorder has germinated more concepts to drive the science of higher cortical functions than have the epilepsies. This brief review will demonstrate that if human brain-behavior relationships learned through study of the epilepsies were removed completely from neuropsychology, there would remain a surprisingly limited foundation for the conceptualization, investigation, and diagnosis of clinical neuropsychological disorders. But the debt actually goes beyond neuropsychology to clinical psychology in general, as is discussed later in this article.
The organization of the peri-Rolandic mammalian cortex into anterior motor and posterior sensory systems is a primary departure point in correlating brain-behavior relationships. A peri-Rolandic motor-sensory zone was inferred by J. Hughlings Jackson (1870) through clinical observations of the morphology and evolution of epileptic seizures in humans. Subsequently, motor zones in the canine cortex were demonstrated experimentally by electrical cortical stimulation (Fritsch & Hitzig, 1870), extended to the monkey and redrawn onto a diagram of human cortex by David Ferrier (1876), and reconfirmed clinically by J. M. Charcot (Gowers, 1885) in epilepsy and stroke patients. However, such localizationist models were antagonistic to the mass action concepts of Munk and Goltz in 1881 (Green, 1985), who demonstrated restitution of motor function following ablation of a primate cortical motor center. This dialectic was debated strongly in neurology and later in psychology (Lashley, 1950), but less in neurosurgery. In 1952, Penfield and Rasmussen published their detailed topographic and proportional maps of the peri-Rolandic motor-sensory cortex in humans. Their cortical homunculus appears in virtually every introductory psychology text (e.g., Seamon & Kenrick, 1992). This homuncular construct was derived almost exclusively through electrical cortical stimulation in conscious patients describing sensations while undergoing neurosurgery for epileptogenic lesions of the brain.
In 1950, R. A. Krynauw, a South African neurosurgeon, performed radical hemispherectomy for treatment of intractable debilitating epilepsy in children. This and subsequent studies of children undergoing left hemispherectomy demonstrated unequivocally that developmental plasticity existed during critical periods of childhood for higher cognitive functions, particularly speech and language (Goodman & Whitaker, 1985). Children undergoing left hemispherectomy can attain near normative levels of speech and language (Smith, 1974), although much controversy exists regarding the duration of the period of plasticity, the amount of behavioral plasticity for specific cognitive functions, the complexity of syntactic development in acquired right hemisphere speech dominance, and numerous other methodological issues (St. James-Roberts, 1981).
Again, an entire field of investigation and the fundamental neuropsychological concept of plasticity for a cognitive function in children was demonstrated empirically through the study of epilepsy. There is no animal analogue for speech and language functions that could have demonstrated this remarkable phenomenon of speech dominance shifting to the neural substrate of the opposite hemisphere. What is the necessary and sufficient neuronal information that triggers the shift to right speech dominance, and what variables within and between the hemispheres promote this shift? Such fundamental questions can be investigated only in epilepsy surgery programs in which hemisphere speech dominance is confirmed empirically through the intracarotid amytal procedure (IAP). No other CNS disorder, including left hemisphere infantile hemiplegia, offers this level of certitude for determining speech dominance or the opportunity to study the attendant CNS effects on cognitive development.
Today, most psychologists know of the critical role of the hippocampal formations in cognitive memory. The hippocampi were studied anatomically for at least a century (see Meyer, 1971) before Scoville and Milner (1957) described cognitive amnesia following bilateral temporal lobe and hippocampal psychosurgery in a psychiatric patient. The critical role of the hippocampi and adjacent temporal lobe systems in memory was confirmed in epilepsy patients undergoing temporal lobectomy for control of intractable seizures (Milner, 1972; Penfield & Mathieson, 1974; Penfield & Milner, 1958). A recent MEDLARS/PsycSCAN literature search resulted in nearly 1,000 references to the index words hippocampus and memory. It was through the study of intractable epilepsy arising within the temporal lobe that the hippocampal formation and temporal lobe structures in cognitive memory were confirmed. This remains a highly active area of research because the exact temporal lobe-hippocampal structures mediating specific aspects of memory are not well understood. For example, bilateral agenesis of the temporal lobes is reported to be associated with normal memory and IQ levels in adults (Lang, Lehrl, & Huk, 1981). However, no review of human memory can be attempted without reference to the role of the hippocampal-temporal lobe complex, and the momentum begun in the 1950s continues nearly 40 years later. Today, neuropsychological studies appraise a patient’s memory and related cognitive functions both before and after temporal lobectomy (National Institutes of Health [NIH] Consensus Development Conference, 1990).
To avoid the devastating human amnestic syndrome following temporal lobectomy, most epilepsy surgery centers conduct the IAP to determine hemisphere speech dominance and memory patency in each hemisphere (Snyder, Novelly, & Harris, 1990) by anesthetization of each hemisphere individually. These determinations are increasingly based on procedures designed and conducted by a clinical neuropsychologist. The IAP is a methodological extension of Wada’s (1949/1985) initial experiment of intracarotid artery injection of sodium amytal in psychiatric patients as a possible procedure to determine hemisphere speech dominance. However, eight years earlier Gardner (1941) locally anesthetized the left cerebral cortex of left-handed patients undergoing neurosurgery to determine the speech dominant hemisphere. Wada’s procedure was expanded to measure hemisphere memory patency by Milner, Branch, and Rasmussen (1962). The IAP was recommended by the NIH Consensus Development Conference (1990) for patients undergoing neurosurgery for epilepsy. This is an active research and practice area, and the IAP outcome is often a central factor in determining a patient’s candidacy for epilepsy surgery and the type of surgery possible.
Conducting the IAP is a privileged clinical and research opportunity for a neuropsychologist. Following hemisphere anesthetization, the reemerging levels of consciousness and stages of aphasia that occur, as each hemisphere clears from the barbiturate, are windows into human brain functions that simply cannot be observed in a patient with a static lesion. The IAP has been used to lateralize the side of a hippocampal lesion (Rausch, 1987), to determine transfer of information between the hemispheres (Rissi & Gazzaniga, 1978), to correlate IAP memory with hippocampal pathology (Sass et al., 1991), and to examine variables related to hemisphere memory patency (Loring et al., 1990).
Currently, it is a virtual dictum that the left and right hemispheres can conceptualize and respond differentially and specifically to sensory information. Levine (1945a, 1945b, 1952), working in Lashley’s laboratory, initially demonstrated hemisphere- and region-specific visual learning in pigeons. This concept of hemisphere-restricted learning, without active or immediate transfer to the opposite hemisphere, was elaborated and verified in higher animals (Russell & Ochs, 1963; Sperry, 1961). The foundation was laid for the related concept that each hemisphere has unique cognitive properties, a distinction already pointed to by studies of patients with focal lesions (Piercy, Hecaen, & Ajuriaguerra, 1960; Teuber, 1962). Neurosurgical commissurotomy of the hemispheres in patients with intractable epilepsy (Bogen & Vogel, 1962) allowed Sperry (1974) to demonstrate empirically, through behavioral procedures, that each hemisphere could conceptualize and respond characteristically to stimulation. This revelation, built on earlier animal work by himself and others, led to the awarding of the 1981 Nobel Prize for medicine to Roger W. Sperry.
From a humble beginning in 1933, when epilepsy first was treated neurosurgically in America by removal and replacement of the cranial cap (Kane, 1950), the subsequent contributions to neuropsychology have mobilized the emergence of neuropsychology as a specialty discipline in psychology.
In clinical psychology, the benefits of using epilepsy as a model disorder have been primarily in the area of temporal lobe epilepsy. Although researchers in this field have been prolific, the investigative results have been inconsistent. When the epilepsies were removed from the category of primary psychiatric disorders, the homogeneity of psychiatric etiology was improved (Zilborg, 1941). However, interchange of concepts between psychiatry and epilepsy research, in efforts to explain disorders in each discipline with concepts borrowed from the other, have been less productive. They include investigations of the epileptic personality (Guerrant, 1962), epilepsy-based aggressivity (Delgado-Escueta et al., 1981), epilepsy insanity defense (Knox, 1968), the “temporal lobe personality” (Rodin & Schmaltz, 1984), epilepsy-psychosis links (Flor-Henryy, 1969), epileptic traits (hypergraphia, religiosity, surliness, and social-emotional characteristics; Bear & Fedio, 1977), and extension of the kindling model of epileptogenesis to psychiatric disorders (Bolwig & Trimble, 1989). To date, none of these concepts have withstood scientific scrutiny. In part, this is because temporal lobe epilepsy is not a homogenous entity simply by virtue of a gross and nominal neuroanatomical geography. Also, psychiatric classifications of pathology are not easily transferable to the epilepsies.
Recent neuroimaging procedures indicating hypometabolism associated with the interictal epileptogenic lesion call for modification of “interictal personality” models in epilepsy, especially those that posit “hyper” forms of behavioral symptomatology. Careful and productive progress in the clinical psychology-epilepsy link is being made (Whitman & Hermann, 1986) by researchers investigating the emotional adjustment problems of persons living with seizure disorders, apparent effects on cognition of chronic antiepileptic medication treatment (Trimble & Reynolds, 1988), and patient compliance with medication treatment (Spilker & Cramer, 1990). Differentiation of pseudoseizures from epileptic seizures, social and occupational limitations of persons with epilepsy, and family adjustment difficulties are additional areas in which clinical psychology has an open opportunity for tremendous contributions. However, only limited work has appeared in the clinical psychology literature on these significant diagnostic and treatment issues.
Hippocrates released epilepsy from the naive status of a “sacred disease” and identified it as brain dysfunction. The debt of psychology to the epilepsies is unique, as the profession would be diminished without the multiple contributions from epilepsy research. Repayment of this debt means continuing efforts to educate psychology students that, far from the caricature of individuals in convulsions with aggressive or other “epileptic personality traits,” the epilepsies present a valuable opportunity to investigate and understand human brain-behavior relationships.