Abstract
Prosopagnosia is a condition during which a face is recognized as such, but not as the face of a person familiar to the observer (1). Patients suffering from this condition recognize their fellow humans by means of their voice, movements, clothing, and so called paraphernalia (glasses, beard, earrings, etc.). Most likely, a dysfunction or lesion of the right fusiform/lingual gyrus is sufficient to cause prosopagnosia, at least transiently. The most common cause is ischaemic, but other causes for disturbed function in the respective region, e.g. tumours, trauma, intoxication, have been reported (2). Here we report the first patient with stereotyped prosopagnostic aura.
Case report
A 58-year-old left-handed man, a tax consultant in his own small firm, was treated in our tertiary care headache centre at Zurich University Hospital. He had suffered from migraine without aura since the age of 20, with an attack frequency of about one per month, with several attack-free periods of a few years. He reported a transient increase in attack frequency around the age of 25, because of which he was put on prophylactic treatment for a few months (no further details remembered). Since the age of 52, all of his migraine attacks had become associated with stereotyped auras, starting with a propagation of ‘coloured rings’, extending from bottom to top in both visual fields, leading after about 10 min to a concentric restriction of the visual fields, sparing more than 45° of central vision. He was unable to specify the colours, but stated that the phenomenon was certainly coloured rather than black and white, without any predominant colour.
At this stage the patient was unable to recognize faces of familiar persons, although he could see them as a whole, and described them as ‘whitish disks’ or ‘eggheads’. To recognize a familiar person he would have to use their voices, movements and clothing. If he was concentrating on a certain part of the face for a while, he was able to recognize it clearly as such (e.g. the nose or the mouth). He could clearly see other parts of the body, the environment, and objects, in colour and had no problem in recognizing them. The prosopagnostic condition lasted an additional 10–15 min, and faded away over about 5 min while the visual field defect normalized. Mental status during such an episode could not be obtained, but in the interval there was no deficit in his status; this included strictly normal face recognition.
Without any interval, there followed strongly pulsating headache of moderate intensity, with a duration of about 12 h when untreated. Headache localization was unilateral in about 80%, and about equally often on each side. In the remaining cases headache was bilateral. It was aggravated by physical activity and accompanied by phono- and photophobia, but no nausea. His usual treatment consisted of analgesics (either 1000 mg of acetylsalicylic acid or a combination of 500 mg paracetamol, 50 mg caffeine and 4 mg chlorphenamine). He reported stress, particularly during work, and weather changes as typical triggers. Since the onset of migraine aura, migraine frequency was higher than before, with several attacks per month. In the 6 months before presentation, on a combination of a β-blocker (nadolol 30 mg/day) and a selective serotonin reuptake inhibitor (fluoxetine 20 mg/day) prescribed by the general practitioner, only three attacks had occurred. About 5 months before presentation to the headache clinic, the patient had suffered a single episode of a typical transient global amnesia, which was diagnosed during a brief hospitalization in our neurology department (normal medical and neurological examination, normal computed tomography).
Family history was negative concerning migraine. His mother died from heart failure at the age of 74, his 49-year-old brother and his 86-year-old father did not have any relevant medical problems. In his past medical history the patient reported having an allergy to penicillin, a tendency to depressed mood during the winter months, an appendectomy and an operation for an inguinal hernia.
Two documented neurological examinations had been normal (when he presented, 55 years old, in the headache unit as well as during his transient global amnesia); apart from slightly elevated blood pressure (about 140/90 mmHg), medical examination was normal, with normal cardiac auscultation and without any rumors over the carotid arteries. Magnetic resonance tomography showed a few small vascular lesions bilaterally in the frontal white matter as well as one small vascular lesion in the right cerebellar hemisphere. Mesiotemporal structures were normal. Neurovascular investigations (Doppler, duplex) were normal, without any signs of obstruction in the posterior circulation. The EEG did not show any abnormalities. Laboratory analyses showed slightly elevated liver enzymes [aspartate aminotransferase 84 U/l (<50); alanine aminotransferase 105 U/l (<50); gamma glutamyl transpeptidase 117 U/l (<61)], and were otherwise unremarkable, as well as a complete cell count.
Discussion
The described headache syndrome fulfils International Headache Society (IHS) criteria for typical aura with migraine headache (IHS code 1.2.1) (3). Stereotypically, the purely visual symptoms are followed in this patient by a neuropsychological condition that equals an episode of prosopagnosia. The patient describes that during these episodes, he is incapable of recognizing the familiarity of a person's face. He reports seeing them as an entity, and perceiving faces of persons he knows as ‘whitish discs’. He is capable of recognizing familiar persons only by means of their movements, voices and clothing and able to recognize single facial configurations. He has never suffered from any form of visual agnosia. The perception of everything else than faces is reported to be undisturbed.
Historically, agnosias were defined as disturbances of recognition with normal perception (4). Later, it was hypothesized that ‘pure’ agnosias are probably non-existent, or extremely rare, and that each disturbance in recognition is accompanied by at least a minor degree of perceptual abnormality (5), mostly scotomas (6).
The term prosopagnosia was introduced by Bodamer in 1947 (7), and is based on the greek words ‘prosopon’ (face) and ‘gnosis’ (recognition). It denominates a disorder in which a face is perceived as such, but without any associated feeling of familiarity. Patients are unable to recognize well-known persons by means of their faces, but are generally able to perceive individual parts of the face correctly (1). Faces are typically perceived as ‘flat’ and, when looking at photographs, it is often not possible to tell whether a picture taken from the side corresponds to a picture of the same person taken frontally; the disorder often includes the inability to recognize even one's own face in the mirror (8).
To enable recognition of persons, prosopagnostic patients use so-called paraphernalia, i.e. glasses, earrings, hair-styles, but also the voice, typical bodily features, gestures and gait as well as clothes.
Therefore, the condition which our patient experiences stereotypically in association with his visual aura is best diagnosed as prosopagnosia, in the absence of other higher visual defects. As, in the centre of his visual fields, he is able to see everything clearly but faces, and his spared tubular field is large enough to allow him to see an entire face at a time rather than just a part of it, the abnormality cannot be attributed to a dysfunction of the eye, or basal visual information processing. Our patient reported visual field defects during his aura, but no abnormalities commonly occurring in association with prosopagnosia when lesions involve a larger part of the cortex, such as object agnosia (with bilateral occipital lesions), achromatopsia (with bilateral medial occipitotemporal lesions), anosognosia (with a lesion, e.g. in area 40 in the parietal cortex) (1).
The localization of disturbed function during the episodes in our patient, at the beginning of the visual aura, with peripheral scotomas progressing to a concentric restriction of the visual fields over about 10 min, is probably in the anterior part of bilateral visual cortices, corresponding to peripheral vision. As only one bilateral symptom is part of the aura, the IHS diagnostic criteria of typical aura with migraine headache (code 1.2.1), rather than those of basilar-type migraine, are fulfilled (3).
Although typical visual auras are commonly thought to be unilateral, a proportion of 30 to over 50% are reported to be bilateral (9–11). Tunnel vision (pronounced concentric restriction of the visual fields) as part of the migraine aura has been described (12) and was reported to occur in up to 10% of visual auras (11).
For prosopagnosia, the typical lesion is the fusiform and/or lingular gyrus in the inferio-medial part of the temporo-occipital junction, mostly on the right side, or bilaterally (2). As this localization is adjacent to the visual cortices, it fits well with the clinical progression from concentric visual field restriction to prosopagnosia.
Due to the episodic nature of the condition, and its stereotypic association with the migraine syndrome, any other aetiology is unlikely in our patient. The time course and stereotypic nature of the episodes, with a gradual onset of visual symptoms over several minutes, gradual progression of the visual aura to prosopagnosia, the duration of 6 yearss as well as normal posterior circulation, make a vascular origin, most common in prosopagnosia, unlikely. For the same reasons, an epileptic origin is unlikely, where, in addition, positive symptoms and/or signs would be expected. The diminished migraine frequency, including the prosopagnostic auras, when on β-blockers is another argument in favour of a migrainous aetiology. Nor can aetiologies of non-episodic nature, such as inflammation, tumour, head trauma, intoxication, etc., explain the condition.
Our patient, having suffered from migraine without aura since the age of 20, experienced aura symptoms for the first time at 52 yearss of age. The Framingham study showed that out of 2000 persons, in 1.33% of women and 1.08% of men, aura symptoms start late in life, but are not associated with an increased risk of cerebrovascular accidents (13).
Although the underlying pathophysiology is unknown, one may speculate that a slightly impaired blood supply due to a certain degree of atherosclerosis might suffice to increase the probability of cortical spreading depression (CSD), the most likely pathophysiological process in migraine aura (14, 15).
Our patient also suffered an episode of transient global amnesia (TGA). Although, the debate is still ongoing, the current understanding tends to favour CSD, rather than ischaemia or epilepsy, as the most likely underlying mechanism of TGA (14), which fits in well with the late occurrence of migraine aura.
With the exception of aphasia, which occurs in up to 18% of migraine auras (16), neuropsychological abnormalities during migraine aura have rarely been described in the literature. There are few case reports on left-hemispheric disturbances, such as agraphia, as the only symptom of migraine aura (17), and alexia without agraphia during migraine aura (18, 19).
To our knowledge, prosopagnosia has never been described as a stereotypically occurring and isolated neuropsychological abnormality as part of a migraine aura. However, there are three reports of patients with prosopagnosia as a part of a complex aura with several neuropsychological abnormalities. Sacks described a 75-year-old female patient in his book on migraine (20), where during the aura phase in a small subset of migraine attacks she experienced a sensation of altered and weakened perception of her body and was unable to identify or point to body parts on verbal instruction (autotopagnosia), a loss of meaning of the objects around her (object agnosia), as well as a change in the character of voices around her (acoustic agnosia), which were sometimes associated with prosopagnosia. Lawden et al. (21) report on two exceptional auras in a female, 49-year-old patient. In one aura a transient achromatopsia was associated with prosopagnosia, and in the second one, object agnosia was followed by prosopagnosia. This patient was reported to have experienced several auras with neuropsychological abnormalities subsequently, but without prosopagnosia. The third patient, reported by Martins et al. (22), experienced a single migraine aura with a complex right-hemispheric dysfunction, with an association of left-sided hemianopia, left-sided paresthesias, loss of topographic memory and prosopagnosia.
In brief, we describe a patient who has previously suffered from migraine without aura and who developed, at the age of 52, stereotypic migraine aura consisting of visual disturbances as well as prosopagnosia.