John Hughlings-Jackson revolutionized the theories of pathophysiology of epilepsy (1, 2). His detailed descriptions of focal motor seizures resulted in the eponym "Jacksonian epilepsy," and he also wrote extensively on another type of epilepsy, which he called the "dreamy state." Carefully collecting case histories throughout his career, he eventually associated the "dreamy state," and its associated signs and symptoms, with the medial temporal region. Using his theories of organization of the nervous system, he also wrote about the implications of the "dreamy state" in human consciousness and thought, leading to concepts that continue to be relevant to ideas of consciousness today.

Many authors have independently outlined Hughlings-Jackson’s writings on the "dreamy state" (1, 3, 4) or his models of consciousness (5–9), but there are no thorough reviews of how he derived his models of consciousness primarily from his observations of the "dreamy state." We reviewed all of Hughlings-Jackson’s published writings about the "dreamy state," summarized these writings, and examined his derivation of degrees of consciousness based on the model of the "dreamy state."

In speaking of classification of the epilepsies, including the "dreamy state," Hughlings-Jackson wrote,

These ideas, far ahead of their time, reflect our concept of epilepsy today (2) and correlate with the current definition of focal (or partial) epileptic seizures as seizures "whose initial semiology indicates, or is consistent with, initial activation of only part of one cerebral hemisphere" (11).

The syndrome of medial temporal epilepsy is a localization-related epilepsy syndrome with associated ictal and postictal signs and symptoms resulting from activation of structures in the medial temporal region (12). Usually, Hughlings-Jackson’s use of the term "dreamy state" was synonymous with our current definition of the ictal and immediate postictal phenomenology of medial temporal epilepsy. However, he also used "dreamy state" to describe a specific symptom, which he believed to be a central feature of what is currently defined as the syndrome of medial temporal epilepsy. In this review we will use "dreamy state" synonymously with the ictal and immediate postictal semiology of medial temporal epilepsy. When referring to Hughlings-Jackson’s use of "dreamy state" as an isolated symptom, we will clarify with the term "symptom of the ‘dreamy state’ " as necessary.

Hughlings-Jackson’s first description of what he termed the "dreamy state" appeared in 1876 (10, 13). Throughout the rest of his career, he continued to publish articles about this variety of epilepsy. He wrote,

This aura is now most often referred to as a feeling of familiarity, or déjà vu. However, Hughlings-Jackson’s broader definition of a heightened intellectual state, or "over-consciousness," is perhaps a better description. With the symptom of the "dreamy state," he further listed associated symptoms of "crude sensations" and at least some degree of alteration of consciousness (10).

Hughlings-Jackson also called the symptom of the "dreamy state" a "double consciousness." In this state, patients were vaguely aware of ongoing events (one consciousness), but were preoccupied with the intrusion of an "all knowing" or "familiar" feeling (a second consciousness) (14, 15). He stated, "This double mental state helps the diagnosis of slight seizures greatly" (15).

Hughlings-Jackson included in his writings many clinical examples of the symptom of the "dreamy state" that are indispensable in understanding the symptom. Hughlings-Jackson based the name of the symptom, the "dreamy state," on a "highly educated" patient’s description of symptoms:

The case of Dr. Z played a central role in Hughlings-Jackson’s descriptions and understanding of the "dreamy state." Dr. Z was a "highly educated medical man" who had the "dreamy state." In 1870, Dr. Z, writing under the pseudonym Quaerens (the seeker), published a brief article (16) quoting Coleridge, Tennyson, and Dickens to describe his symptoms. Dr. Z wrote detailed descriptions of his own seizures, reported by Hughlings-Jackson in 1888 (17, 18). Eventually, it was determined that Dr. Z was actually Dr. Alfred Thomas Meyers, a physician at the Belgrave Hospital in London, with whom Hughlings-Jackson was acquainted (3, 4). Meyers died in 1894 from an overdose of chloral (a class of sedative medication, used in modern-day medicine as chloral hydrate). Hughlings-Jackson participated in Meyers’ autopsy, finding a "very small patch of softening in the left uncinate gyrus" (18).

Dr. Z’s description of his first seizure was,

Dr. Z described his own clinical events, shedding light on the nature of the symptoms of "double consciousness," as follows:

Intrigued about the accuracy of his diagnosis, rendered during the "dreamy state," Dr. Z proceeded as described below.

Hughlings-Jackson also commented on patients’ attitudes toward their seizures. In a minority of cases, patients found the "dreamy state" pleasurable and would attempt to bring on the symptom (10, 19). He also noted a consistency of symptoms, quoting Falret: "These ideas, these remembrances, these false sensations, which differ singularly in different patients, are generally reproduced with remarkable uniformity in the same patient at each new attack" (20).

In addition to the symptom of the "dreamy state," Hughlings-Jackson observed other symptoms, which he referred to as "crude sensations" (10, 15). He considered them to be in the spectrum of the symptom of the "dreamy state" but much less elaborate. They included the following (10, 15): 1) "paroxysms beginning by an epigastric sensation," 2) "fear (rarely anger)," 3) "paroxysms beginning by noises in the ear," 4) "fits beginning by colored vision," 5) "taste," and 6) "a crude sensation of smell."

Hughlings-Jackson wrote that the "crude sensations" could occur before, during, or after the symptom of the "dreamy state." During a particular seizure, "crude sensations" and the symptom of the "dreamy state" could occur together or as isolated symptoms. Hughlings-Jackson postulated a relationship between the type of "crude sensations" and the symptom of the "dreamy state" but was unable to establish this from his case histories (10, 15).

Hughlings-Jackson described ictal symptoms of pallor, sweating, tachycardia, lip smacking, and chewing movements. He considered lip smacking and chewing movements to be related to other gastrointestinal symptoms (such as the common aura of an epigastric sensation):

Hughlings-Jackson wrote extensively on postictal states, outlining many clinical cases. He appreciated the varieties of symptoms after seizures, ranging from "giddiness attended by trivial confusion of thought" to a "full violent seizure with universal convulsion and deep coma" (21).

In describing psychic symptoms, especially mania, in epileptic patients who had no discernible ictal event, he wrote,

In reference to the "dreamy state," Hughlings-Jackson listed several scenarios of postictal actions, including continuance of actions ongoing before the seizure ("although in an imperfect and perhaps grotesque way"); disorientation and mild delirium, sometimes associated with wandering; the "so-called coordinated convulsion," with struggling, shouting, and kicking, "often taken for hysteria"; and the patient’s becoming "violently maniacal" (15).

Hughlings-Jackson associated mania, as he did the symptom of the "dreamy state," with epileptic seizures that impair consciousness as an initial manifestation:

In 1873, Hughlings-Jackson wrote about seizures characterized by a "sudden stench in the nose, with transient unconsciousness" (20). He stated that such symptoms were localizable but that he was unable to localize them at that time. Hughlings-Jackson eventually correlated the "dreamy state" and postmortem examination in several cases (including the case of Dr. Z [18]). In what proved to be some of the final publications of his career, through clinicopathological correlations he linked the "discharging lesion" of the "dreamy state" to the medial temporal region in what he called the "uncinate group of fits" (17). Of his localization of the "uncinate group of fits," he wrote,

As outlined above, Hughlings-Jackson described and localized the syndrome of medial temporal epilepsy with his descriptions of the "dreamy state." However, his interest in the "dreamy state" went beyond the characterization of the syndrome. He saw the study of epilepsy as a key to understanding brain organization and function, stating, "No better neurologic work can be done than the precise investigation of epileptic paroxysms" (10). Integrating ideas from his study of neurological disease as a whole (but primarily from his study of the "dreamy state") and his theories of organization of brain function, Hughlings-Jackson formulated his ideas about consciousness.

Hughlings-Jackson built on the ideas of Thomas Laycock, stating that all neurological functions relied on sensory and motor reflexes (20). The sensory and motor functions were represented most simplistically at the spinal ganglia, with phenomena such as the deep tendon reflex as an example. Hughlings-Jackson saw the brain as being regulated by laws identical to those governing the spinal ganglia. The brain, "although the organ of consciousness, is subject to the laws of reflex action, and…in this respect, it does not differ from the other ganglia of the nervous system." Hughlings-Jackson also emphasized that higher nervous system function involved representations of sensory and motor processes rather than actual sensory and motor functions. The representation of sensory and motor processes he called "sensori-motor" function. "Sensori-motor" functions were represented and rerepresented, in greater complexity from the lowest to highest nervous system centers:

Following the teachings of Herbert Spencer, Hughlings-Jackson proposed evolutionary levels of nervous system function (14). Functional levels increased in complexity and interconnectivity with evolution. A given function was represented and rerepresented at different levels, in its simplest form at the lowest level and its most complex form at the highest level (19). The clinical consequence of this hierarchical system was that CNS lesions induced both negative and positive neurological symptoms. A lesion (or "dissolution") in the highest levels resulted not only in negative symptoms attributable to a loss of higher function but also in positive symptoms attributable to release of a lower level from inhibitory control. A clinical example is thalamic pain syndrome, where a loss of sensation represents a loss of a higher level of somatosensory function, while constant pain represents the unmasking or release of a lower level of function (5).

Hughlings-Jackson noted the clinical association of the "crude sensations" in epilepsy to loss of consciousness:

Pulling together his ideas of the association of the "dreamy state," the "crude sensations," postictal symptoms, and loss of consciousness, Hughlings-Jackson proposed functioning levels of consciousness. He noted the disparity in the elaborateness of the "dreamy state" and the rudimentary nature of "crude sensations." He thought of the symptom of the "dreamy state" as representing a higher degree of consciousness and "crude sensations" as representing a lower degree of consciousness.

Using the model of epilepsy, Hughlings-Jackson described three degrees of consciousness:

In keeping with his ideas about the positive and negative elements of dissolution, he proposed such elements in each degree. In the first degree the positive state was the "dreamy state," while the negative state was a degree of loss of consciousness (realities misperceived). In the second degree the positive state was the "crude sensations," while the negative state was complete loss of postevent recollection of ongoing ictal events. In the third degree the positive state was mania, and the negative state was coma (14, 23). Hughlings-Jackson also related the degrees of consciousness to his ideas of subject and object consciousness (t1).

Hughlings-Jackson commented on the difficulties of defining consciousness, pointing out that the assessment of consciousness in an individual patient was subjective. He stated that observations can be made only on how one interacts with one’s environment, and that trying to affix a definite state of consciousness is a psychological and not a physiological question. Rather than defining consciousness, he emphasized that reestablishing phenomena associated with defects in consciousness was of much greater practical importance. He built his model of consciousness by studying deficits of consciousness in patients with diseases of the brain, using his theories of sensorimotor phenomena and dissolution. He expressed the advantages of this approach as follows:

Using his ideas of sensorimotor function, Hughlings-Jackson described two "halves" of consciousness, a subject half (representations of sensory function) and an object half (representations of motor function). To describe subject consciousness, he used the example of sensory representations when visualizing an object (23). The object is initially perceived at all sensory levels. This produced a sensory representation of the object at all sensory levels. 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 sensory information of the initial perception of it.

What enables one to think of the object? This is the other half of consciousness, the motor side of consciousness, which Hughlings-Jackson 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. Hughlings-Jackson related subject and object consciousness as follows:

Hughlings-Jackson saw the two halves of consciousness as constantly interacting with each other, the subjective half providing a store of mental representations of information that the objective half used to interact with the environment.

In relating consciousness to the "dreamy state," it is important to understand that Hughlings-Jackson was referring to abnormalities of consciousness occurring during the ictal and postictal states—not interictal states, when there is presumably normal consciousness. He further defined the terms "subjective" and "objective," relating them to symptoms of seizures, as follows:

Hughlings-Jackson tied the ideas of subject and object consciousness to the degrees of consciousness represented by the "dreamy state":

Expressed another way, Hughlings-Jackson saw a relative decrease in object consciousness and a relative increase in subject consciousness during the dreamy state; these represent changes in the first degree of consciousness. He did not describe the object and subject consciousness relationship of ictal phenomena at lower degrees, but one may infer that at the second degree of consciousness, the complete loss of postictal recollection of ictal events represents a further deficit of object consciousness, while the "crude sensations" represent an increase in the second degree of subject consciousness. At the third degree of consciousness, coma represents an even further deficit of object consciousness, while mania represents an increase of the lowest degree of subject consciousness. t1 lists the relationship of the signs and symptoms of the "dreamy state" to changes in degrees of consciousness.

Hughlings-Jackson recognized that his definition of brain function based on sensorimotor phenomena could not explain associated mental phenomena. In 1873, he wrote,

Hughlings-Jackson developed his theory of concomitance to relate mental and nervous states. In 1884, he wrote,

From his definition of concomitance, it is evident that Hughlings-Jackson considered epilepsy to affect the nervous state, which, through a different but parallel mechanism, produced a change in the mental state of consciousness.

Hughlings-Jackson’s teachings about consciousness have influenced psychiatry. His writings about subject consciousness likely influenced Freud’s ideas of the "subconscious" as well as Freudian psychopathology (6, 25, 26) and continue to be applied today in discussions of psychiatric issues (27). The influence of Hughlings-Jackson’s writings on Freud must be inferred because Freud rarely credited any sources for his ideas (28). Before he wrote on the subject of psychoanalysis, Freud wrote a book on aphasia based on Hughlings-Jackson’s writings (28). As with most of his writings, Hughlings-Jackson’s articles on aphasia relate his neurological findings to his ideas of organization of the nervous system, including consciousness (6). Harrington (28) made a convincing argument for similarities of Hughlings-Jackson’s ideas of subject and object consciousness and Freud’s idea of primary/secondary thought, positing that the concept of "pathological subject consciousness" was the basis for Freud’s ideas about repression.

Hughlings-Jackson’s description of the "dreamy state" describes the signs and symptoms of medial temporal epilepsy essentially as we understand them today. His postulations about a "discharging lesion" in the medial temporal region causing the symptoms also predate the current pathophysiologic concept of localization-related epilepsy. Subsequent developments of ictal electroencephalography recordings, however, have revealed one notable error in his postulations about symptoms in the "postictal" state. Hughlings-Jackson’s "mental automatisms" and "postictal actions" often begin during epileptic discharges and may or may not persist into the immediate postictal period (29). Whether positive symptoms in general, ranging from simple repetitive movements to the complex motor automatisms as presented in the history of Dr. Z, represent a direct activation of neuroanatomical structures from an epileptic discharge or are the result of a "release" allowing emergence of a lower degree of function remains an issue of debate (29, 30).

Hughlings-Jackson described "release" phenomena with his theory of evolution and dissolution of the nervous system, which is now often referred to as "hierarchies" of nervous system function (31). That positive symptoms occur during the ictal discharge of the seizure does not rule out a "release" phenomenon causing them, given the concept that discharging neurons are dysfunctional to some degree. Advances in functional neuroimaging, especially the emergence of ictal single photon emission tomography (SPECT), which enables measurement of ictal blood flow changes (which correlates with ictal electrical discharges [32]) over the entire brain, will likely help to resolve this issue (33). Consciousness in epilepsy has already come under study with ictal SPECT, and initial studies correlate loss of consciousness with secondary activation of bithalamic and upper brainstem structures (34).

A critical review of the concept of consciousness in epilepsy by Gloor (35) reveals an approach to defining consciousness that contrasts with Hughlings-Jackson’s approach. Gloor drew on epistemological and scientific arguments to attempt to define consciousness, which he admitted may never be possible, to illustrate that such definitions provide little to further our understanding of epilepsy. Hughlings-Jackson circumvented many of the difficulties in defining consciousness by using changes induced by neurological diseases (primarily epilepsy) to define it. Gloor described the complexity of consciousness and proposed that aspects of conscious experience such as perception, cognition, memory, affect, and voluntary motility are open to neurobiological research. The concept that consciousness is complex is very much in agreement with the ideas of Hughlings-Jackson. Indeed, Hughlings-Jackson’s conceptual framework for consciousness and epilepsy addresses many of the questions that Gloor raised. Especially relevant to psychiatry is the study of affective states.

As well described by Hughlings-Jackson, medial temporal epileptic seizures produce affective symptoms that are repeatedly and stereotypically seen in individual patients. The ictal and immediate postictal symptoms of medial temporal epilepsy, therefore, provide a pathophysiological model to study affective symptoms. Hughlings-Jackson’s description of the "dreamy state" integrates affective symptoms into an overall scheme of organization of the nervous system. The difficulty of interrelating "physical" and "mental" symptoms of consciousness, especially in the realm of affective symptoms, continues to be an important issue (36). Hughlings-Jackson proposed a method to do so, relating the "physical" and "mental" phenomena of the "dreamy state" with his theory of concomitance. The progression of Hughlings-Jackson’s thoughts about concomitance, in which he attempts to address the issue of "psychology versus physiology" in defining consciousness, mirrors the progression of modern neuroscientific thought, in which there is no longer a distinction between psychology and physiology. In the complex realm of defining consciousness (37), Hughlings-Jackson’s theories provide an interesting perspective for correlating brain function with mental function that may provide useful concepts for interpretation of modern investigations of human brain function, helping to better understand the functional basis of neuropsychiatric disease.

Of continued clinical interest is the issue of complex peri-ictal behavior. Of the complex peri-ictal behaviors, aggressive behavior is a particular concern. In a thorough review, Treiman (38) concluded that peri-ictal aggressive acts were stereotyped, simple, unsustained, and not supported by a consecutive series of purposeful movements. Treiman reported that "resistive violence," where attempts to restrain patients still in a postictal confusional state produce violent reactive automatisms, is the most common phenomenon associated with aggressive behavior. He stated, "It is probable that such resistive violence occurs as a result of differential recovery of functional areas of the brain such that there is a relative delay in the recovery of pure motor functions." The incidence of peri-ictal aggressive behavior is rare, but it occurs commonly enough to be a clinical concern (39). Most investigators emphasize that the clinical situation, especially reaction of bystanders during the peri-ictal state, is one of the most important factors in provoking aggressive behavior (38, 39).

Putting this phenomenon in the framework of Hughlings-Jackson’s classification of consciousness is helpful in understanding it. Hughlings-Jackson’s first degree of subject consciousness is associated with misperception of realities. Patients misperceive the intentions of bystanders during resistive violence and react to what they perceive as threatening behavior. A clear understanding of this phenomenon is important when evaluating patients with aggressive behavior, especially when the patient has a history of epilepsy.

Hughlings-Jackson not only described and localized medial temporal epilepsy but used his findings to help establish his theories of consciousness. His insightful description of the semiology of medial temporal epilepsy remains a useful reference. His innovative thoughts about its implications in consciousness provide an interesting model of brain function that remains relevant to contemporary ideas about consciousness. However, Hughlings-Jackson’s interrelation of the "dreamy state" and consciousness remains largely unrecognized. Further investigations of this relationship may continue to shed light on epilepsy as a model of brain function and elucidate the mind-brain relationship.

Received Feb. 11, 2002; revisions received Nov. 1, 2002, and April 10, 2003; accepted April 29, 2003. From the Greater Midwest Epilepsy Treatment Center, Department of Neurology, Saint Louis University School of Medicine. Address reprint requests to Dr. Hogan, Greater Midwest Epilepsy Treatment Center, Department of Neurology, Saint Louis University School of Medicine, 3635 Vista Ave. at Grand Blvd., St. Louis, MO 63110; hoganr2@slu.edu (e-mail).