History of frontal lobe seizures

Any historical review of seizures originating in the frontal lobes (FLS) is faced with several difficulties: the huge diversity of ictal manifestations, from the most simple myoclonic event originating in the elementary precentral motor cortex, to very bizarre and misleading phenomena, involving associative cortices and widely distributed networks, that were not rarely misinterpreted as psychogenic attacks (Tharp [1] ); the often unclear relationship between semiologic patterns and sublobar localization in spite of many attempts to characterize typical anatomical-clinical-electrical patterns that would be typical of a given sub region, like the orbito-frontal or medial frontal lobe areas [2] , [3] ; the different terminologies employed to characterize FLS, reflected in the evolving classifications of the International League Against Epilepsy (ILAE) between 1981 and 2017. FLS are often brief, sometimes a few seconds, due to the rapid propagation pathways which are offered inside and outside the frontal lobe to the epileptic discharge, making the observation and the analysis difficult, although seizures in a given patient with frontal lobe epilepsy are generally stereotyped, with a stable and reproducible electro-clinical pattern. And last but not least, FLS are often nocturnal, without obvious electroencephalographic (EEG) correlations, and have been often in the past misdiagnosed as parasomnia. The manifestations include: paroxysmal arousals, characterized by brief and sudden recurrent motor paroxysmal behavior; nocturnal paroxysmal dystonia, motor attacks with complex dystonic–dyskinetic features; and episodic nocturnal wanderings, stereotyped, agitated somnambulism. The recognition of their epileptic nature led to the terminology of Nocturnal Frontal Lobe Epilepsy, and a familial clustering permitted the discovery of several pathogenic gene variants [4] , [5] . In spite of this complexity, the study of frontal lobe seizures has largely contributed to our understanding of the pathophysiology of epileptic discharges: the first description of focal clonic seizures by J.F. Bravais in 1827, then Hughlings Jackson in 1867, who related clonic seizures to electric discharges in the contralateral precentral region and described a “march”, this stepwise invasion of neighboring areas of the motor cortex by the ictal discharge, with progressive somatotopic engagement of limb musculature. Other frontal lobe seizure types, however, showed that this march phenomenon cannot be considered as a universal model of emergence and spreading of the discharge. Supplementary motor area seizures producing speech arrest (a negative phenomenon), unilateral arm posturing, and head or eye deviation, later referred to as “fencing posture” by Penfield [6] , illustrate rapid modalities of subcortical propagation. Using stereoencephalography, Bancaud and Talairach [2] defined frontal lobe automatisms, and detailed descriptions of complex partial seizures of frontal lobe origin followed with P. Williamson et al. [7] . The term “hypermotor seizure” was also proposed. In the revised ILAE classification, FLS are classified as “focal seizures” with further descriptors such as “either aware or with impaired awareness”, or “with or without observable motor components” [8] . Frontal lobe seizures with secondary generalization are now described as focal evolving to bilateral tonic-clonic seizures.