Abstract
In the International Headache Society classification of headaches, the concept of aura is given a key role. It serves as a boundary between ‘migraine without aura’ and ‘migraine with aura’. Historically, the concept of an aura was borrowed from the epilepsy vocabulary; a borrowing that took place in English medicine at the beginning of the 19th century and in French medicine in the mid-19th century. It would therefore be interesting to see which features of the epileptic aura are used to explain the migraine aura. Based on the French and English medical literature of the 19th century, two processes have been reviewed: (i) the emergence of the concept of aura, and (ii) the modifications of this concept throughout the 19th century. It appears that the original medical use of the term ‘aura’ as a set of rising tactile sensations was in use from the 2nd century until late in the 19th century, but then various other symptoms were recognized and the aura gradually became accepted as an early part of the seizure. By the end of the 19th century the aura that preceded a migraine was seen as a similar process, and thought of as part of the migraine sequence.
Introduction
The coexistence of two concepts of aura in modern neurology is a potential source of misunderstanding. Are these concepts reciprocal? To what extent can we, legitimately and productively, point out similarities between migraine aura and epileptic aura?
Migraine aura is defined by the International Headache Society (1) as a set of neurological symptoms that usually occur when the migraine headache starts, or immediately precede it. This aura nearly always includes (2) visual phenomena, which may be associated with somatosensory manifestations, and sometimes motor symptoms, psychic manifestations in the form of memory, and language dysfunction (3).
A number of vascular and neurological hypotheses have been put forward to explain these phenomena. The neurological hypothesis (4, 5, 6) that is now predominant, is based on a model of the wave of ‘spreading depression’, which can be triggered experimentally anywhere on the cerebral cortex (7).
About the sense of the term ‘aura’, the IHS classification of 1988 was rather ambiguous; the aura ‘initiates or accompanies an attack’; it ‘does not necessarily imply that it precedes the headache’; it is the ‘beginning of an attack of migraine’. Since the 19th century, it has been said that migraine aura phenomena may occur during or after the attack of headache. But according to the hypothesis of cortical spreading depression, the primarily cortical phenomenon, responsible for the aura symptoms, may activate trigeminovascular fibres and, by this way, contribute to migraine headache. How explain, then, that aura symptoms may occur after pain? Two studies suggest that headache and aura are simultaneous only in 4.7–7.4% (8, 9); headache is recorded to occur before aura symptoms in about 2.7–11.1% (8, 9); in this last case, the authors think that the attacks may be explained by ‘an attack of tension-type headache followed by an attack of migraine with aura rather than biological variation of the attacks’ (8).
The epileptic aura, according to the Commission on Classification and Terminology of the International League Against Epilepsy (10) is nothing more than that part of the seizure that happened prior to the loss of consciousness and is therefore remembered. This concept of memory and awareness was already mentioned by Marchand and Ajuriaguerra (11). Symptoms of the epileptic aura are varied: autonomic symptoms, special sensory symptoms (auditory, gustatory, olfactory, vertiginous), cephalic symptoms, motor symptoms, somatosensory symptoms, psychic symptoms (12, 13).
From a pathophysiological perspective, the epileptic aura is the ‘result of a functional cortical zone activation (such that this zone will determine the aura features) by an abnormal, unilateral, localized short neuronal discharge’ (14). Therefore, as Hughlings Jackson assumed at the end of the 19th century, it identifies the area of the brain that is the source of the seizure: an excessive discharge of nerve tissue ‘began in a local region of the cerebral cortex and might spread from its area of origin to involve other parts of the brain. The spread of the discharge correlated with the development of further seizure manifestations’ (15).
Despite similarities, one major distinction should be drawn between epileptic and migraine auras: there is no relationship between the durations of the two types of auras; this may be an indicator to discriminate between a simple partial seizure (lasting only a few seconds to up to 2–3 min), and a migraine with aura not accompanied by headache (at least 5 min).
The explanations currently suggested for these manifestations allow us to assume that they may have a different nature. This had lead Sheryl Haut to say that ‘it is unfortunate that the term “aura” is used in both migraine and epilepsy, because they represent different entities’ (16).
How did the concept of an aura pass from epilepsy to migraine? What where the consequences of this importation?
Popular source of the word ‘aura’
The Historical Dictionary of the French Language (17) reminds us of the various usages of the word ‘aura’ and of its etymology. According to the Encyclopédie méthodique (1790) (18), the latin phrase aura epileptica, abbreviated as aura, is derived from the latin term aura, which means ‘breeze’ or ‘atmosphere’, which is a poetic or literary borrowing of the Greek word aura (a breeze, a whiff, a waft, an odour), from which the French word ‘orage’ (‘storm’) is derived. Although there seems to be no certainty in the derivation, it has been thought that the Greek word aura may have come from the word aêr, which led to aero, and ‘air’. At the end of the 19th century and under the probable influence of ‘aureole’ (in the sense of a halo), ‘aura’ also meant, in French, a ‘halo which could only be seen by initiates’ in the field of occult sciences; by extension, it came to mean a ‘mysterious atmosphere’, a condition of visibility which paradoxically becomes visible. In French, the gender of the word is usually feminine but the ‘Trésor de la langue française’ states that ‘some authors attribute a masculine gender to aura, fostered by the vocalic initial of the word’ (19).
During the first half of the 19th century, the mysterious quality in the lay use of the word was always part of the medical meaning, so that the idea of an aura often carried, for some physicians, a notion of oddity, a supernatural feeling, a ghostly quality, something one is unable to explain (20).
The etymology of aura indicates an elusive feeling (wind, breeze), which has no obvious connection with visual hallucinations, motor or even psychic feelings. It is, primarily, a tactile feeling, which does not mean that the Greeks did not know many other premonitory signs, as Temkin shows (21, 22). Let us go back to the story with which Galen introduced this concept in the history of medicine. There are three types of epilepsies.
‘All without exception [hapasôn autôn] have therefore this in common, that the encephalon is affected, either because the disease is generated there (…), or because it moves up from the opening of the stomach (…), by sympathy, to the encephalon (…). Another epilepsy type or genus or variety may occur, though rarely, depending on how you want to call it: the disease starts in any part of the body, then climbs up towards the head in a manner that the patient himself can feel. When I was young, I saw this phenomenon for the first time in a 13-year-old boy (…). I heard the child tell that the condition [diathesis] had begun in his leg, and then had gone up straight to his neck, going through the thigh, groin, ribs, and neck up to the head; as soon as his head was reached, he lost consciousness of himself. When questioned by the physicians about the nature of what he felt moving up to his head, the child was unable to answer. Another young man, who was intelligent enough, capable of feeling what was happening to him and more able to explain it to others, answered that a sort of cold breeze [auran tina psukhran] was rising in him. Hence, Pelops, my Master, concluded it had to be one of two things, either something rose up towards the head, by being passed from one structure to an adjacent part, or it was a pneumatic substance [ê pneumatikê tis ousia]’ (23).
Though it has been variously interpreted, this passage does go on to submit that the three types of epilepsy are brain disorders: the first sort, which has its seat and origin in the head and the brain, is the one that tradition called epilepsia ex capite or ex cerebro. The second sort, epilepsia ex ore ventriculi, is an epilepsy, which, though it is seated in the brain, has its cause and origin in one of the soft, fluid-containing internal organs of the body. Finally, epilepsia ex parte externa or epilepsy coming from one limb, also has its seat in the brain, but it has its cause and origin in an outer part. As Boissier de Sauvages explained it, symptoms of the aura ‘have their origin in the brain or in the principle of nerves which serve for the use of that part, as are the imaginary aches that those who had their leg or thigh amputated a long time ago may feel in their foot’ (24). Formed in the brain, these sensations are manifest in the rest of the body. It was said at the end of 19th century that the aura was the ‘peripheral effect of a central lesion’ (25).
Tradition hesitated between a phenomenological conception of aura, and a causal one. Boissier de Sauvages, for example, thought of the aura as an imaginary sensation, whereas Brown-Sequard (26) was in the causal school.
Anyhow, Galen evokes it, first, as a feeling, but calls it an ‘attack’ because the patient can feel it. He then asserts that it is ascending sensation, and that it may have its origin in any part of the body.
As can be seen from these accounts, the idea of aura was not, originally, a scholarly or theoretical idea but one that was brought into medicine by way of the patients' complaints (27).
Pelops's first patient was unable to define this feeling. The aura was such a vague and uncertain complaint that it was often dismissed (28). The second patient gave an approximate description (further indicating the difficulties in defining this sensation). This phrase was translated into Latin as aura quaedam frigida: ‘a sort of cold vapour’. In fact, the aura, as it was introduced in medical tradition, does not sound like a cacophony from multiple sensory sources, it suggests rather a single hard-to-define feeling, going beyond language.
Pelops, Galen's teacher in Smyrna, tried to express his thoughts about these cases by considering two possibilities: either there is (i) a transmission of an unknown quality or sensation, that was passed up the body from one affected part to an adjacent part (in this case the aura (the feeling rising up through the body) is only a manifestation, merely the expression of the transmission); or (ii) or there is a transmission of some pneumatic substance. If this is the case, then the aura is ousia, it has some substance, and there is more hope that there is a cause to be found.
Pelops and Galen left the issue pending, and over centuries medical tradition has hesitated between the two hypotheses, being sometimes in favour of a ‘manifestation’, and sometimes in favour of some ‘substance’, that is, some cause. Galen was given credit for these ideas, although he is not known to have written anything else about it (29).
Herpin, in 1852, collected a series of modifications of these ideas. For instance, the notion of aura was contaminated by that of venom, probably because Pelops had proposed a ligature as therapy for the aura (perhaps because a limb ligature was also used to delay the rising effects of a snake bite): aura was soon descried as a ‘cold and corrupted vapour such as the venom of harmful beasts’ (30). Other physicians substituted the idea of some cold thing for that of a ‘chill vapour’ (30). Words like ‘matter’ and ‘spirit’ (spiritus) are substituted for ‘vapour’. Starting in the 18th century, the use of the term aura quaedam frigida began to fade and it was replaced by diversified feelings: a sort of flame, a tingling, painful spasms, convulsions.
In 1790, the Encyclopédie méthodique defines aura epileptica as something that moves, a running fluid, an insect that dawdles towards the head (18). Esquirol reported associated symptoms of convulsions and pain (31). Chaussier described it as a particular feeling, a sort of shudder or movement (32). For Pinot, it was just an imaginary sensation of movement (33). The 1830 edition of the Encyclopédie méthodique reported one case with painful ringing in the ears (34).
Up to 1830, the phenomena that were regarded as aura were mainly of a visceral (ascending feeling) or somatosensory type (heat, cold, pain); we also have a description of auditory hallucination (painful ringing), and one description of motor phenomena (convulsion, spasm). Cognitive and affective elements of the psychic auras, as well as simple or complex visual hallucinations, are missing.
Most commonly, the aura is described as tactile and centripetal (35): ‘When the sense of touch is the seat of hallucination, the term “aura epileptica” is used to describe it’ (36).
First classification of aura manifestations
This early interpretation of the aura (a vague, variable, but chiefly tactile sensation rising through the body to the head) lasted until the end of 19th century; the term ‘aura’ also appears in Féré's writings in 1891 (37) and he was a man who made a major contribution to the history of migraine and epilepsy. A second meaning then appeared, under the decisive influence of Herpin and Delasiauve. They did not think of an epileptic aura as a single undefined sensation, but as a variable cluster of sensations. As says Temkin, ‘With (…) the connection of the term “aura” with symptoms of a quite different character, the way was now opened to an identification of “aura” with all possible warnings' (38). The aura that was experienced and described by the patient was a composite made up of several separate auras. This made it necessary to set up a phenomenology and a classification.
In the article on ‘epilepsy’ in the Dictionnaire de médecine ou répertoire général des sciences médicales (1835) Georget offers a long list of apparently unrelated symptoms extending far beyond the limited primary meaning of the word ‘aura’: ‘sometimes, immediately prior to the attack, some patients have odd hallucinations, hear an unusual noise, see luminous objects, smell foul odours, taste particular flavours, feel a sort of blow, in the head, heart or stomach (…). Some are seen spinning on their feet, or running and then falling. A patient feels that the attack is about to come, calls for help, looses the ability to speak, feels his head and limbs twisting, finally loses consciousness. Here is what we have seen.’ The authors then add the following: ‘They speak of aura epileptica, which manifests itself by a feeling of cold, freshness, heat, shivering, tickling, numbness, pain, etc., in a part of the body more or less distant from the brain, i.e. at the vertex of the head, in a lip, the breast, a limb, the foot, hand, or finger tips, etc. The patient immediately feels a sort of movement or vapour coming from this area and moving towards the brain, sometimes going through the heart and the stomach’ (39).
It sounds as if the concept of an epileptic aura had become too narrow to give a clear account of the experience. Herpin, however, came to that very conclusion in 1852, in Du pronostic et du traitement curatif de l'épilepsie, and after him, Delasiauve, in 1854, in his Traité de l'épilepsie.
Delasiauve made the distinction between an aura and a prodrome. He used an analogy, later made famous by repetition, in which he compared the prodromes to the signs that herald an approaching storm (heaviness of the air, suffocating heat, turbulence of heavy clouds) and he compared the aura to the early stages of the storm itself – flashes of lightning and thunder claps (40). This analogy is made almost inevitable, by the history of the words because the Greek word aura led to the French word orage, meaning a storm. Prodrome and aura are both heralding signs, warnings. The prodromes have no necessary relationship with the attack, but the aura cannot be distinguished from the attack, and the patient recognizes this and identifies the aura as ‘an integral component of the attack’ (41).
Delasiauve is considered to be the first who made the distinction between motor, sensory, sensitive and intellectual auras (42, 43). From Herpin and André we get a considerable list of sensory auras: there were sensations of warm or cold vapour affecting an area on a limb or on the trunk (according to Herpin (44), the aura frigida represented only 1% of the total aura symptoms he recorded). There were feelings of numbness, tingling, pain, the sensation of having a ball going up to the neck as in the hysterical aura, and various kinds of psychic distress including auras with odd or incongruous behaviours, depressive state, decrease of intellectual abilities, memory loss, involuntary terrors, rages, sudden changes in feeling and mood. Occasionally there were some complex structured hallucinations, hyperesthesias, photophobia, blindness, coloured tinted vision, the appearance of known or imaginary persons, macropsia, micropsia, diminished hearing, hyperacusis, voices calling insulting words, perception of sparks, haloes, objects moving forward or backward creating a feeling of breathlessness in the patient. There were quite a few unpleasant olfactory and gustatory sensations, and abdominal complaints including: vomiting, epigastralgia colic, oppression, sensation of a weight in the stomach, constriction, pressure, stomach ache, and, interestingly an ‘abdominal aura’ (45) sui generis as an expression of a seizure activity. This kind of thing may have led to the cautionary maxim: ‘Render unto seizure the things which are seizure's, and unto gut the things that are gut's' (46).
Jules Voisin distinguished between affective auras (depression, anxiety, obsession, sense of persecution) and intellectual auras (reminiscence, ‘sort of dream’, aphasia). In an article from the Nouveau dictionnaire de médecine et de chirurgie pratiques (47) Auguste Voisin equally reported an aura consisting of a ‘feeling of well-being’ much like those described by Dostoevsky in The Idiot (48).
Epileptic aura and migrainous aura
According to Liveing, the analogy between the epileptic aura, and some manifestations of migraine go back, in the English language tradition, to the beginning of the 19th century: ‘it is impossible not to be struck by the apparent resemblance of these phenomena – the tingling and its centripetal progress – to the so-called aura epileptica; Sir James Clark has remarked upon it in a passage in which he clearly identifies the malady of which we are treating as “Nervous Dyspeptic Headache”: “In some cases the attack is preceded by numbness in the extremities, by dimness of sight, or ocular spectra; in others a peculiar uneasy sensation, originating in one of the extremities, ascends gradually to the heads, resembling the aura epileptica” ' (49).
In 1841, Babington also reported a case of sick-headache: ‘it is remarkable (…) that it [the epileptic aura] is not necessarily connected with epilepsy at all (…). A near relative of my own furnishes an example. He is much subject to headaches, dependent on a disordered state of stomach (…). These attacks are often ushered in by a sensation of tingling in one arm, which mounts up from his fingers’ end, and gradually advances towards the face on the same side, affecting one half of the tongue, palate, and lips' (50).
In France, the use of the word ‘aura’ in relation to migraine appeared much later. Whereas in England, it directly reflected the ancient and limited meaning of the word ‘aura’ (the aura being understood as a tactile sensation), the French term fluctuated between this meaning, and a much laxer definition corresponding, more or less, to the second meaning of the epileptic aura concept (i.e. that the aura is the early tip of the seizure ‘iceberg’ that protrudes into consciousness and is recognized and remembered).
The oldest occurrence I have found in the French literature appears in 1859, in a medical doctoral dissertation by Allory (51) in which ‘aura’ refers to the starting point of the migraine. In order to describe the zigzag visual hallucinations, the dazzling, blindness episodes, the occasional horripilation, yawning, a sense of hunger, deafness, excessive cold, tingling, numbness, and the temporary paralysis of the limbs or tongue, Allory classifies all of these phenomena as ‘prodromes’ of migraine.
In fact, a number of French physicians do not distinguish between ‘prodromes’ and ‘aura’ (according to Friedlander, this is a common characteristic of modern epileptology) (52); this allows them to classify any condition preceding a headache, as an aura, this last concept being then strictly chronological. For instance, Soula wrote in 1884: ‘Just as all operas have an overture getting the spectator ready, and a book has its foreword to inform the reader of the situation, so each migraine has its foreword, or overture, which corresponds, in a way, to the epileptic patient's aura. This aura (…) may show endless variations (…). What one should never forget, is that migraine always has an aura; it is mandatory … and free of charge' (53).
Archipoff in 1888 remarked that the aura of migraine was elusive, sometimes almost imperceptible, it may be limited to a malaise, fatigue, nausea or, conversely, there may be an unusual alertness, or even nightmares (54).
Chaumier, in 1878, reminds us that Liveing considered the aura as being made chiefly of tactile disorders: tingling, numbness, anaesthesia, hemiplegia, chills, or a cold sensation (55). But, for Chaumier, the aura belonged to a much larger class of nervous disorders, and also included motor manifestations (convulsions of the limbs and eyelids) and psychic manifestations (speech, memory and consciousness disorders). Pleading in favour of a wider meaning of the aura concept, Chaumier broke up the synonymy between prodrome and aura, noting that in migraine, the aura could occur at any time during the attack. He also made an effort to demonstrate that some auras had no links with ‘tactile’ disorders; he reported cases of speech and memory problems, and some word articulation difficulties, with no concomitant tingling; he also recalled the case of Sir G. B. Airy (the father of Hubert Airy) who suffered from episodic scintillating zigzag visual disturbances, occasionally associated with brief impairment of speech, and memory loss, but without headache. Chaumier also drew the timeline and spatial relations between aphasia, visual disorders and tactile disorders (pricking, tingling, numbness): for instance, did these last conditions occur in only one side (and if yes, which side is the most frequently affected?) or in both sides? Did visual disorders and tactile disorders occur on the same side?
The psychic conditions reported by Chaumier are, without a doubt, one of the first mentions of the ‘déjà-vu’ and ‘dreamy state’ sensations in migraine: ‘anything the patient sees and hears, appears to him as having already been seen and heard in a dream. He experiences a feeling of emptiness around him; he feels he is no longer in a close relation with external objects and that something is standing between them’. Distortion in the determination of time is equally found in the aura: ‘It seemed to him that the past was the present, and the present was confounded with the past’. These psychic disorders, and the ‘double consciousness’ they envelop, and the analogy with the well-known excerpt from David Copperfield, had already been reported by Liveing, but were not among the symptoms of the aura, considering the restricted meaning that he gave to the concept (56).
Among the supporters of the original and limited meaning, Soudry restricted the notion of aura to include only tingling, numbness and semi-paralysis. Two case reports persuaded Soudry that these manifestations could reach the domain of speech: one stated that the migraine episode ‘always began with a visual disorder, but subsequently one arm and one leg on the same side were paralysed, and then by turns one day on one side, the next day on the other side. Then the same thing occurred in the mouth and tongue, in conjunction with a great difficulty in speaking’. The other report said: ‘Migraine started with numbness which, from the small finger of the hand, moved to the tongue and resulted in an extreme difficulty in uttering words’ (57).
Conclusion
The very old concept that most epileptic seizures were preceded by some kind of tactile ‘aura’ was gradually extended to hemicranial headaches when, in the 19th century, it was recognized that migraines also came with a warning aura. This transfer of the epileptic aura to the migraine aura began in England in the 1830s and 1840s, and in France in the 1860s (unfortunately, I have very little information on the evolution of this concept in German-speaking countries). In the English-speaking tradition, the transfer was uneventful, but in the French tradition a new concept arose from the work of Herpin and Delasiauve, which is still undergoing a number of changes.
The aura of epilepsy. Starting in about 1852–1854, the ancient idea, that epileptic auras were exclusively tactile, was rejected. The concept was then rebuilt to include a wide variety of manifestations borrowed from diverse fields but having one thing in common: they immediately precede, and are an integral part of the seizure, and often reveal something about the location of the problem in the brain.
The aura of migraine. The reconstruction of the concept of the aura epileptica was not without an impact in the field of migraine. A series of visual, motor and psychic disorders do often occur before a migraine headache. They warn of its approach but they do not seem to say much about the location of the problem. They are simply ‘prodromes’, they do nothing except precede and foretell the headache. The concept of the migrainous aura as it is developed in 19th century France suggested that it shared a mechanism with the epileptic aura. It was a useful term for the doctor who needed a name for a clinical phenomenon, but it was not otherwise helpful. It did not shed light on any possible mechanism, and the term was usually an ill fit: either too narrow or too wide. Although it was used in students' dissertations, it was not picked up by the Faculty. Piorry (58) in 1831 called it ‘ophthalmic migraine’, but it still lacks a rigorous definition.
In the lack of the hypothesis of the spreading depression, migrainous aura was only an analogical term. Unlike epileptic aura, it did not involve localization. The idea that the symptoms may begin in a localized cortical area only appears in the first half of the 20th century, with Leão.
Acknowledgements
I would like to express warm and grateful thanks to Professor H. Stanley Thompson for his critical remarks.