The different patterns of seizure-induced aphasia in temporal lobe epilepsies
Introduction
It has long been known that seizures arising from the dominant temporal lobe of the language-dominant hemisphere may elicit speech disturbances. Paroxysmal dysphasia was associated with left hemisphere lesions by Jackson [1]. In the premonitoring era, this phenomenon was described in a patient with left temporal lobe epilepsy who became seizure-free after temporal lobectomy [2]. Later, based on video-EEG recordings, seizures arising in left temporal lobe were shown to be strongly associated with postictal language disturbance [3], [4], but ictal aphasia or dysphasia was not precisely characterized.
In addition, the overlap between loss of consciousness and language disturbance is a difficult problem, which is not easy to resolve, and may explain why in some studies left TLE have been more frequently associated with loss of consciousness than right TLEs [5].
In the last ten years, detailed evaluation of consciousness using multiple criteria scales have been proposed to evaluate loss of consciousness and distinguish this from language impairment [6], [7], [8]. The different proposed consciousness rating scales included (1) nonverbal response (orientation, gestural interaction), (2) verbal response (e.g., ability to follow commands requiring verbal answers, naming), and (3) the ability to recall events that occurred during the seizure.
Although aphasia may be the most prominent or sole manifestation of seizures [9], [10], the description of its semiology remains vague, and even if changes in semiological terminology have been made, recommending that partial seizures should be now described according to their “dyscognitive” features [11], ictal aphasia has been included in the automatism section. “Dysphasic seizure” is, thus, described as “impaired communication involving language without dysfunction of relevant primary or sensory pathways manifested as impaired comprehension, anomia, paraphasic errors, or a combination of these” [12]. No distinction has yet been proposed between the different patterns of ictal aphasia, as it has been described in stroke [13].
In a review of ictal aphasia, Benatar pointed out that the literature on this topic is relatively scant and most of the papers included in the review dealt with status epilepticus [9]. On the basis of several well-studied reported cases, the author concluded that potentially any type of aphasia might occur as an ictal sign. In addition, seizures do not seem to predominantly produce any single type of aphasia. Finally, it is difficult to establish a straightforward correlation between the type of aphasia and location of the epileptogenic zone.
The lack of data about ictal aphasia could be explained by the difficulty of testing and evaluating language during the brief and transient state of a seizure.
The aims of the present study were (1) to describe the different patterns of ictal aphasia in temporal lobe seizures and (2) to identify precise anatomoelectroclinical correlations using intracerebral recordings (stereoelectroencephalography, SEEG) defining the contribution of different regions (including temporal lobe regions but also frontal and insular regions) involved in temporal lobe seizures with ictal aphasia. The SEEG approach allows sampling of multiple distant areas included in the network language with high spatial and temporal resolution. To differentiate loss of consciousness from speech disturbance, we selected seizures with early clinical testing and with preserved nonverbal interaction (that is, excluding seizures with significant loss of consciousness using the operant definition). The aim was to establish specific electroclinical patterns.
Section snippets
Patients
Among stereoelectroencephalographic (SEEG) recordings obtained from patients between 2008 and 2014 who underwent presurgical evaluation of drug-refractory temporal lobe epilepsy in our epilepsy monitoring unit, we retrospectively selected seizures according the following inclusion criteria: (1) occurrence of ictal speech disturbance; (2) early ictal examination of patient permitting assessment of consciousness and language during the 30 first seconds of seizure; (3) consciousness level
Results
As an initial step, we analyzed the expert agreement. For SEEG data, the agreement of seizure analysis between the two neurologists (AT and FB) was excellent (Cohen's kappa1 = 0.94). For the clinical evaluation of language, the agreement between the three clinicians was excellent for 8 items out of 13 (Cohen's kappa between 0.84 and 1.00), and good for 3 items (between 0.69 and 0.73).
Discussion
Elucidating electroclinical correlation of ictal aphasia is an important issue during presurgical evaluation. This study is the first to use a detailed electroanatomical approach to evaluate ictal aphasia during TLE seizures, describing three main patterns of ictal aphasia. All selected patients and seizures benefited from detailed ictal testing of both language and awareness within the 30 s after the seizure onset. Until now, the scarcity of data on ictal aphasia could be indeed explained by
Conclusion
In conclusion, it is possible to distinguish three main patterns of ictal aphasia according to the sublobar temporal region involved during the seizure: (1) impaired speech comprehension was associated with posterior lateral involvement; (2) anomia and low fluency with anterior mediobasal structures; (3) and jargonaphasia with basal temporal involvement. A more important consideration is the fact that language production deficits in the present study, such as anomia and low fluency, cannot be
Acknowledgment
The authors thank all the nurses of the epilepsy unit for the ictal language testing, the neurosurgeons, Jean Regis, Henry Dufour, and Didier Scavarda, for presurgical (SEEG) and surgical procedures, and F-Xavier Alario for his helpful comments.
This work was supported by the Brain and Language Research Institute (Aix-Marseille Université: A*MIDEX grant ANR-11-IDEX-0001-02 and LABEX grant ANR-11-LABX-0036) and by the FHU EPINEXT (Aix-Marseille Université: A*MIDEX project, ANR-11-IDEX-0001-02).
Disclosure of conflicts of interest
None of the authors has any conflict of interest to disclose.
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2022, Handbook of Clinical NeurologyCitation Excerpt :MTLE and FLE-like seizures in TPE may highlight the regional propagation—toward MTL or frontal structures—of the epileptic discharge. Several studies have also described aphasic focal aware seizures in TPE involving the dominant hemisphere (Toledano et al., 2013, 2016; Trebuchon et al., 2018). Some authors have emphasized that aphasic seizures arising from the temporal pole are not necessarily explained by the propagation over perisylvian language areas (Broca's and Wernicke's areas), and may also result from the involvement of anterior temporo-basal structures, i.e., the “basal temporal language area,” which is located 2–9 cm from the tip of the temporal lobe and includes the fusiform gyrus (Lüders et al., 1991; Trebuchon-Da Fonseca et al., 2009; Toledano et al., 2013; Trebuchon et al., 2018).
Temporal lobe epilepsy: A never-ending story
2021, Epilepsy and BehaviorCitation Excerpt :This must not be astonishing given the demonstrated role of the pole and basal anterior temporal cortex in mesial TLE [44], structures that play a significant role in language function. It must be highlighted that Trébuchon et al [42] included 8 patients with an anteromesial EZ in their stereo-EEG study of ictal aphasia; their systematic clinical exam during the seizures unveiled in these patients a pattern of initial transcortical aphasia followed by impairment of both emission and comprehension. The infrequent but feasible maintenance of visual and verbal interaction during the seizures, even in the presence of automatisms, is illustrated by 2 (11.1%) of our patients with right non-dominant mesial TLE.
Epileptic aphasia – A critical appraisal
2021, Epilepsy and BehaviorCitation Excerpt :Another study demonstrated that the presence of a structural lesion significantly prolonged postictal language delay only in the patients with nondominant temporal CPS, supporting a complex interaction between seizure origin and patterns of seizure spread [101]. Certainly, the characterization of different patterns of language or speech disorders is helpful in analyzing the anatomo-electro-clinical correlations [102]. There are some caveats, such as preserved language in language-dominant left temporal lobe epilepsies.
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2021, NeuropsychologiaCitation Excerpt :Additionally, we observed that left TLE patients made more semantic errors than controls, and, interestingly, more omissions than controls and right TLE patients (Rice et al., 2018; Woollams and Patterson, 2018). This pattern of word retrieval deficits occurring in conjunction with semantic paraphasias has been previously associated with damage in the left temporal pole, and aligns with the proposal that left ATL has a crucial role in lexical access (Q. Chen, Middleton and Mirman, 2018; Lambon Ralph, McClelland, Patterson, Galton and Hodges, 2001; Mesulam et al., 2013; Poch et al., 2016; Trebuchon et al., 2018). In any case, these deficits were not as severe as those observed in SD or stroke-related aphasia (Mesulam et al., 2013; Schwartz et al., 2009; Woollams and Patterson, 2018).