Localization Value of Somatosensory Auras: History
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Ana Leticia Fornari Caprara
,
Jamir Pitton Rissardo

An aura is a subjective experience felt in the initial phase of a seizure. Studying auras is relevant as they can be warning signs for people with epilepsy. The incidence of aura tends to be underestimated due to misdiagnosis or underrecognition by patients unless it progresses to motor features. Also, auras are associated with seizure remission after epilepsy surgery and are an important prognostic factor, guiding the resection site and improving surgical outcomes. Somatosensory auras (SSAs) are characterized by abnormal sensations on one or more body parts that may spread to other parts following a somatotopic pattern.

  • aura
  • seizure
  • epilepsy
  • focal epilepsy
  • EEG
  • MRI
  • somatosensory

1. Introduction

The term aura denotes the subjective symptoms at seizure onset that the patient perceives [1]. Aura means “breeze” and probably has its roots in Roman and Greek mythology, where “Aura” was a Goddess, a daughter of the Titan Lelantos and Periboea. She is raped by Dionysus and becomes the mother of twins. She maintains a blinding rage to the point of madness throughout pregnancy and tries to kill her children, which culminates in the murder of one of them. Then, a sequence of suicide attempts leads to her final plunge into the river Sangarius, where she is transformed into a spring [2].
In the 2nd century AD, Aretaeus (Aretaios), a physician born in Cappadocia, was one of the first to describe aura phenomena. His meticulous observational approach resembled distantly the modern medical scientific methods. He wrote books about several diseases, including epilepsy. He described “(…) an olfactory aura and sluggishness, vertigo, heaviness of the tendons, plethora and distension of the veins in the neck, and much nausea (Book 1, Chapter 5) and: But, if it be near the accession of the paroxysm, there are before the sight circular flashes of purple or black colours, or of all mixed together, so as to exhibit the appearance of the rainbow expanded in the heavens; noises in the ears; a heavy smell; they are passionate, and unreasonably peevish. They fall down then, some from any such cause as lowness of spirits, but others from gazing intently on a running stream, a rolling wheel, or a turning top. But sometimes the smell of heavy odours, such as of the gagate stone (jet), makes them fall down” [3][4]. One of the earliest descriptions of an aura has also been made by Galen, one of Aretaeus’ contemporaries, around 200 AD [5]. Historically, the aura was referred to as all prodromal symptoms before the seizure onset [6].
The International League Against Epilepsy (ILAE) characterizes an aura as a seizure with certain motor, sensory, autonomic, or psychic phenomena without losing consciousness [7]. It can be prolonged on rarer occasions, constituting a form of status epilepticus [8]. Aura is generally associated with focal aware seizures; however, it could occur right before focal impaired awareness seizures and in generalized seizures [9]. Auras can be experienced as negative or, more commonly, positive sensory symptoms. Positive symptoms include paresthesia, visual and auditory hallucinations, and somatosensory illusions. On the other hand, negative symptoms include numbness, deafness, blindness, and inability to move a body part [10].
The prevalence of aura can be considerably variable, ranging from 22% to 83% in epilepsy patients. Individuals with active epilepsy can report auras more frequently [5]. In a large study on 798 epilepsy patients, around 65% of patients reported having auras [11]. In Gower et al., a series of 2013 cases revealed that around 57% had an aura [12]. In another series of 1527 cases, about 56% of patients experienced an aura. The Epilepsy Phenome/Genome Project (EPGP) study revealed that women were more likely to report auras. However, this may be attributed to the larger number of older women compared to the other groups. Studying auras is extremely relevant as they can work as warning signs for people with epilepsy, increasing their sense of self-control of the disease and allowing them to take rescue treatments in seizure emergencies. Developing new drugs for rapid epileptic seizure termination is a pressing need, and the study of auras and prodromes in epilepsy plays an essential role in this field [11][13].

2. Auras Is an Important Localizing Element of the Epilepsy Foci

It was John Hughlings Jackson (1835–1911), an English neurologist, who first established a correlation between seizure symptoms and the location of the lesion [14]. Historically, before the era of advanced technologies and imaging modalities, surgeons primarily relied on ictal manifestation to identify the epileptogenic area for resection. Accordingly, auras, as the first symptoms of seizures, were an important localizing element of the epilepsy foci [15]. Later, intraoperative cortical stimulation provided a comprehensive method for epilepsy surgery [16][17][18]. Previous studies have established an association between somatosensory auras and the somatosensory homunculus. When there is an epileptic zone in the SI cortex, unilateral and distal sensory auras could occur. However, when the SII area is activated, this could result in bilateral symptoms [19].
There is an essential issue to remember in determining the location of lesions that cause seizures. Ictal discharges are generated in the epileptogenic zones in the brain and only manifest on spreading to other areas. Those areas which can produce symptoms are called symptomatogenic zones [20]. Thus, it is crucial to recognize the possible propagation pathways to be able to determine the area of origin of seizures. However, some symptoms may overshadow other minor clinical manifestations. Therefore, in patients who experience one type of symptom, it does not necessarily mean no ongoing ictal activities in other areas [10][21].
According to multiple studies, the most common localization for somatosensory auras is in the upper extremities, followed by the lower extremities and the face [22][23][24][25]. The hand specifically was the most frequent initial site, which reflects the wide cortical presentation of the hand [26].
In a French study by Mazzola et al., pain and somatosensory responses to direct intracerebral stimulations were acquired in subjects referred for epilepsy surgery. Percentages of somatosensory response in the SI (93.5%) and SII (83.0%) were significantly higher than that observed in the insula (64.0%) (p = 0.03) [27].
Palmini et al. investigated the localizing significance of auras in 179 patients with focal seizures. The study was performed with a retrospective and prospective cohort. In the retrospective group, 123 surgically operated patients had been followed up with electroencephalograms (EEGs) for four decades. The prospective group was comprised of 56 patients with DRE. The researchers found thirty-two patients (twenty-four from the retrospective group and eight from the prospective group) with SSAs. One individual had temporal seizure onset, nine frontal, and twenty-two parieto-occipital from these. In the retrospective series, there was an association between SSAs and sites of seizure onset in one patient with temporal onset, eight patients with frontal, and fourteen patients with parieto-occipital onset. Seven out of eight patients with SSA in the prospective group had a final diagnosis of parieto-occipital epilepsy. Three individuals had only parieto-occipital spikes, two had parieto-occipital and temporal spikes, and the other had no interictal spikes [28].
Perven et al. retrospectively reviewed 333 patients submitted to TLE surgery between 2005 and 2010. From these, 26 (7.8%) individuals had SSAs. Ten patients with SSAs underwent invasive evaluation before surgery, with nine undergoing subdural grid with some depth electrodes. Only one patient underwent stereo-EEG. Almost half (twelve patients) had unilateral sensory symptoms, with three reporting symptoms ipsilateral to the epileptogenic zone, whereas nine patients reported contralateral symptoms. Among the most frequently reported sensations were tingling and numbness. Some individuals also mentioned “warmth”, “cold”, and “sizzling”. When compared to patients who were submitted to surgery straight away, patients who underwent invasive evaluation with subdural grids or stereo-EEG were more susceptible to presenting with seizures after surgery on multivariate analysis, although they sustained similar seizure freedom. According to the researchers, these results may be due to poorer prognosis epilepsies in those individuals that require invasive EEG. According to the researchers, these results may be attributed to more complicated epilepsies with discordant preoperative diagnostic data in patients who eventually required invasive EEG [29].
Yamamoto et al. reported a case of a 52-year-old right-handed Japanese man who had invasive EEG performed due to DRE presenting with focal seizures. The individual reported experiencing numbness in the upper left back that extended to the upper and lower left limbs. Brain magnetic resonance imaging (MRI) revealed a round calcified lesion in the right Sylvian fissure. Implanted subdural electrodes and ictal ECoG studies demonstrated low-voltage fast activities starting only from an electrode on the right inferior parietal lobule. There were no ictal activities observed in the parietal operculum electrodes. Somatosensory evoked potentials were detected in the ictal onset zone located caudal to the perisylvian area. Therefore, seizures originating from the inferior parietal lobe may result in focal seizures that exhibit ictal semiology and scalp EEG results similar to those originating from the second SSA. Noteworthy, this research showed that the sensory cortical representation has a high degree of connectivity with different brain areas [23][30].
A German retrospective study assessed localizing features of individuals with focal epilepsy who reported SSAs at seizure onset. Interestingly, all subjects reported somatic sensations described as dysesthesia, numbness, pain, temperature changes, and tingling. Of the 75 participants of the study with interictal and ictal surface EEG, 32% had parietal foci, 22% had a focus anterior from the frontocentral region, and 13% had temporal foci. In contrast, 20% did not localize the focus on the EEG well, 6% had vertex foci, and 5% had opercular foci. In 44 individuals, unilateral extremity auras were reported and were associated with a centro-parietal EEG focus in 36 patients and a lesion in that region in 30 patients. Bilateral extremity or axial auras were reported in 31 patients. From these, there was a correlation with a centro-parietal region EEG onset in twelve patients, temporal cortex in six, vertex in seven, and diffuse foci in six patients. In 38 individuals, the SSA remained localized without march, followed by a motor pattern. In 30% of the patients, postural tonic and psychomotor seizures occurred. In only six percent of the individuals, unilateral tonic seizures were associated with the SSA in the upper extremity and a contralateral central parietal focus. Subjects with diffuse or hemispheric lesions reported negative motor features. In 17%, generalization with tonic–clonic motor features was observed. In thirty-seven patients, the SSA progressed with a march, occurring in the upper extremity in 46% and leg in 12%. A hemicorporal spread occurred in 24%, and a truncal spread in 14% of the subjects; however, contralateral spread over the midline was rare and was only seen in 2% [23].
Matsumoto et al. reported an adult man with focal cortical dysplasia (FCD). They explored epileptogenesis mechanisms by paired-pulse direct cortical electrical stimulation. Electrocorticograms (ECoGs) were performed, and corticocortical evoked potentials (CCEPs) were obtained by averaging ECoGs recorded from the surrounding areas. Subdural electrodes were placed for invasive monitoring of the patient’s left foot primary somatosensory (SI) and motor areas. The patient experienced an SSA, which evolved into a left leg clonic seizure. During this period, single and paired stimulation at the focus showed increased cortical excitability defined by enlarged CCEP and decreased intracortical inhibition, which suggested increased intrinsic epileptogenicity during seizure generation [31].
A Korean study investigated the clinical features and the diagnostic sensitivity of brain MRI, interictal/ictal scalp EEG, positron emission tomography with 18-F-fluorodeoxyglucose (FDG-PET), and ictal single-photon emission computed tomography (SPECT) in patients with parietal lobe epilepsy (PLE). Forty patients who were diagnosed with PLE between 1994 to 2001 were included. To diagnose PLE, there should be either a discrete lesion in the parietal lobe on brain MRI with ictal EEG or an exclusive ictal onset zone in the parietal lobe confirmed by intracranial EEG. A total of 27 patients underwent surgery. Surgical outcomes were defined as “seizure-free” or “non–seizure free” and “favorable” or “unfavorable”. Seizure-free was considered when there was seizure remission after surgery, including the absence of auras. The postoperative seizure frequency should decline by more than ninety percent to be considered a positive outcome. A video EEG monitoring system recorded interictal/ictal scalp EEGs in all patients. Intracranial EEG monitoring was performed in twenty-seven cases with inconclusive or discordant results. The placement of the grid or strip was determined by the results of ictal scalp EEG, PET, ictal SPECT, and clinical semiology. Pre- and intraoperative functional mapping and intraoperative ECoG were also performed when necessary. A total of 27 of the 40 patients experienced at least one type of aura before a seizure [32].
The Korean study showed that SSAs were the most frequently (13, 32.5%) reported auras. SSAs were contralateral to the side of the seizure in ten (25%), bilateral in two (5%), and ipsilateral to the side of the seizure in one (2.5%) patient. The affective aura was the second most frequent type, which was experienced by six (15%) patients, followed by vertiginous (four, 10%), visual (four, 10%), autonomic (three, 7.5%), and gustatory (three, 7.5%) auras. Among the forty patients, twenty-seven underwent operative surgery. Parietal neocortical resection was done in twenty-one subjects, simple lesionectomy in five patients, and lesionectomy with marginectomy in one patient. Among the twenty-six patients who underwent surgery with more than one year of follow-up, twenty-two (84.6%) had a favorable surgical outcome, including fourteen (53.9%) seizure-free patients, whereas four (15.4%) patients had an unfavorable outcome. Ictal EEG correctly localized the lesion in five of the fourteen seizure-free patients and five of the twelve non-seizure-free patients. Ictal EEG lateralized the epileptogenic hemisphere in six patients. Ictal EEG was falsely localized to the temporal, occipital, or frontal electrodes in seven individuals. Non-lateralization was found in one patient [32]. In 14 remittent patients, interictal scalp EEG did not localize the epileptogenic lobe. In four patients, interictal EEG lateralized the epileptogenic hemisphere. However, seven individuals presented with non-lateralization, including three patients with a normal interictal EEG. Additionally, interictal EEG was falsely localized to three patients’ temporal or frontal electrodes [32].
Salanova et al. assessed 82 patients with non-tumoral PLE treated surgically at the Montreal Neurological Institute between 1929 and 1988. The study’s main objective was to identify the clinical manifestations, ECoG, results of cortical stimulations, and prognostic factors. Pre-excision ECoG was performed in 63 patients and postresection in 46 patients. A total of 80 patients underwent intraoperative cortical stimulation. ECoG was continued during stimulation. It was found that 94% exhibited aura, of which SSAs (55.3%) were the most frequently reported. The epileptogenic zone was contralateral in fifty-one individuals and bilateral in one individual. Thirteen of the fifty-two subjects described pain, and five reported a thermal sensation. Nine subjects reported disturbances of body image, of which 33.3% mentioned a sensation of movement in one extremity, and one individual described the absence of one leg. A total of 66 patients had surface EEG, and seizures were recorded in 36 [15].
The fronto-centro-parietal region (22 out of 66, 33%) was the most commonly observed location of interictal epileptiform discharge. The other areas associated with abnormal electrical activity were the parietal-posterior-temporal (14%), parietal (14%), parieto-occipital (9%), fronto-centro-temporal (4.5%), fronto-temporal-parietal (4.5%), hemispheric maximum posterior head region (9%), bilateral (4.5%), and no epileptiform discharges (7.5%). On the other hand, secondary bilateral synchrony was described in 32% of the individuals. Most cases revealed a lateralized ictal discharge, but it was also observed over the centro-parietal and posterior head regions. In four patients, there was localized parietal seizure onset. A total of 80 patients underwent intraoperative cortical stimulation. Auras were reproduced in 44 out of 80 (55%) patients, which were more commonly referred to as a tingling sensation. Furthermore, 43 patients had right parietal corticotomies. Pre-operative ECoG showed spiking in the following regions: superior parietal (eleven), inferior parietal (eleven), fronto-centro-parietal (five), and opercular region (nine), no epileptiform discharges (two), and unavailable data (five). In seven out of thirty-six (19%) patients, spiking was also recorded from the posterior-superior-temporal region [33].
Left parietal corticotomies were performed in 39 individuals, but only 25 had ECoG data. The spiking patterns were: superior parietal (14), inferior parietal (one), opercular region (four), upper supramarginal gyrus (two), posterior-temporal-parietal (one), posterior parietal (one), parieto-occipital (one), and no epileptiform discharge (one). Post-resection ECoG was available in 46 patients: 26 (57%) had either no spiking or a significant reduction of spiking, and 20 out of 46 (43%) had residual spiking. Furthermore, 79 individuals had a complete description of the follow-up, in which 23% became seizure-free after early attacks, 21.5%% had worthwhile improvement, 20% were seizure-free since surgery, 14% had no improvement, 10% had rare seizures since surgery, 9% were initially seizure-free with late recurrence of rare seizures, and 2.5% had only auras. Therefore, 65% of patients benefited significantly from surgery [33].
Afif et al. studied intracerebral electrical stimulation in patients with epilepsy to evaluate the anatomo-functional organization of the insular cortex. Twenty-five individuals with drug-resistant focal epilepsy were submitted to insular cortex stereotactical implantation of at least one electrode. Sixty-seven stimulations induced at least one clinical response. Eighty-three responses were evoked from insular cortex stimulation. The main responses were sensory, motor, pain, auditory, oropharyngeal, speech disturbances, and neurovegetative phenomena. Regarding somatosensory responses, 10 patients mentioned 11 responses (13.2% of all responses and 28.2% of responses evoked by stimulation sites within the posterior insula) contralateral to the electrical stimulation (ES) site. Three responses were reported in the upper limbs, three in the lower limbs, and one in the neck. Five of these seven responses were evoked by ES in the non-dominant hemisphere, the remaining two in the dominant hemisphere. Electrodes located in the postcentral insular gyrus were responsible for all responses. Following stimulation, four warmth sensations were reported by four patients. From these responses, three were achieved by ES of the postcentral gyrus, two occurred in the cranium, and one in the contralateral elbow. The ES of the middle posterior long gyrus of the posterior insula resulted in one response where the individual mentioned warmth in all four limbs [34].

This entry is adapted from the peer-reviewed paper 10.3390/medicines10080049

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