Investigating the Anterior Temporal Lobe With Direct Intracranial Recordings.

Anterior temporal lobectomy, also known as cortico-amygdalohippocampectomy (CAH), is one of the most effective operations for medically intractable (“pharmacoresistant”) epilepsy and can be associated with a greater than 70% chance of seizure freedom in patients with temporal lobe epilepsy1-3. Despite the potential for an excellent seizure outcome after CAH, resection of language dominant anterior temporal lobe (ATL) is frequently associated with a pronounced and specific deficit in naming4. Neuropsychologically, deficits can be seen as a decline in visual confrontation naming (e.g., naming concrete entities as on the Boston Naming Test4), but the most striking deficits (and those that are most troubling to patients) are in proper naming of unique entities (e.g., famous faces as on the Iowa Famous Faces test5) and in learning new proper names. Lesion studies have provided consistent evidence that proper naming (e.g. of famous faces, landmarks) is dependent on the language dominant ATL6, 7. Interestingly, studies comparing CAH to selective amygdalohippocampectomy (where the ATL is partially disconnected, but spared) report no significant difference in cognitive decline between the two techniques8. In contrast, recent reports examining naming outcomes following selective laser ablation of the amygdala and hippocampus (a technique that spares ATL connectivity) report better postoperative naming outcomes9. Together, these findings suggest that language dominant CAH-associated naming impairment is a result of ATL resection or disconnection. Although the nature of CAH-associated naming impairment is well-studied, the physiologic mechanisms of naming in the ATL are poorly understood and are difficult to study using noninvasive techniques. One reason for this is the variation in ATL response patterns in functional magnetic resonance imaging 10, which may be attributed at least in part to signal dropout caused by susceptibility artifact that is particularly prominent around the ATL11, 12. Positron emission tomography has also been used7, 13, but is limited by low temporal resolution that cannot resolve the exquisite timing of language processes. Therefore, studying the physiologic correlates of cognition in the ATL is technically challenging, and noninvasive techniques to map ATL language cortex with high spatial and temporal resolution are not yet available. Recently, there has been increasing use of intracranial electrodes, which are implanted in patients with medically intractable epilepsy for localization of epileptic foci, to directly study the physiology of the ATL with excellent spatial and temporal resolution. An emerging body of literature14-17 demonstrates the utility of intracranial recordings for studying ATL physiology and has yielded important results that have increased knowledge about ATL function. Traditionally, coverage of the ATL has been achieved with an anteromedial strip electrode that provides sparse coverage of ATL cortex18. Recently, we developed a specialized electrode array that fits within the middle cranial fossa to provide dense and consistent coverage of ATL cortex for localization of both epileptogenic and eloquent cortex14. In this manuscript, we describe our preliminary work studying physiologic responses of the ATL during proper naming.

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