Electrocorticographic functional mapping identifies human cortex critical for auditory and visual naming

Abstract

More comprehensive, and efficient, mapping strategies are needed to avoid post-operative language impairments in patients undergoing epilepsy surgery. Conservative resection of dominant anterior frontal or temporal cortex frequently results in post-operative naming deficits despite standard pre-operative electrocortical stimulation mapping of visual object (picture) naming. Naming to auditory description may better simulate word retrieval in human conversation but is not typically tested, in part due to the time demands of electrocortical stimulation mapping. Electrocorticographic high gamma (60–150 Hz) activity, recorded simultaneously through the same electrodes used for stimulation mapping, has recently been used to map brain function more efficiently, and has at times predicted deficits not anticipated based on stimulation mapping alone. The present study investigated electrocorticographic mapping of visual object naming and auditory descriptive naming within conservative dominant temporal or frontal lobe resection boundaries in 16 patients with 933 subdural electrodes implanted for epilepsy surgery planning. A logistic regression model showed that electrodes within traditional conservative dominant frontal or temporal lobe resection boundaries were significantly more likely to record high gamma activity during auditory descriptive naming than during visual object naming. Eleven patients ultimately underwent resection and 7 demonstrated post-operative language deficits not anticipated based on electrocortical stimulation mapping alone. Four patients with post-operative deficits underwent a resection that included sites where high gamma activity was observed during naming. These findings indicate that electrocorticographic mapping of auditory descriptive naming may reduce the risk of permanent post-operative language deficits following dominant temporal or frontal resection.

Introduction

Patients with debilitating pharmacoresistant partial seizures arising from the dominant hemisphere may be candidates for epilepsy surgery. This procedure often follows intracranial monitoring with implanted subdural electrodes to identify appropriate surgical boundaries by mapping the epileptogenic zone and functional language cortex prior to resection. The current gold-standard for language mapping in this setting is electrocortical stimulation mapping (ESM), during which a small electrical current is sequentially passed through adjacent electrodes and inhibition of function is interpreted to indicate functional language cortex. ESM has been shown to provide accurate mapping of visual object naming (Anderson et al., 1999, Hamberger et al., 2001, Krauss et al., 1996, Sinai et al., 2005b). However, studies have also shown that avoiding visual naming regions alone does not prevent all post-operative language deficits (Cervenka et al., 2011b, Davies et al., 2005, Hamberger et al., 2005, Kojima et al., 2012, Sinai et al., 2005b), and in one study over 50% of patients had post-operative language deficits despite ESM of language prior to surgery (Davies et al., 2005).

Researchers have postulated that auditory descriptive naming, during which patients respond to auditory stimuli such as “an instrument you beat with sticks”, rather than naming an object, is a more “ecologically valid” measure of naming than visual object naming since individuals encounter naming by auditory description more frequently during normal conversation than naming of objects (Hamberger and Seidel, 2003, Hamberger et al., 2005). Auditory descriptive naming requires not only utilization of a different sensory modality, but also sentence and syntax processing, which are not utilized during visual object naming. Therefore, one plausible explanation for why patients experience post-operative language deficits despite mapping of visual object naming is that regions responsible for sentence and syntax processing may not be comprehensively mapped or preserved.

Studies demonstrate that ESM can also interfere with auditory descriptive naming (Hamberger et al., 2001, Hamberger et al., 2005, Kojima et al., 2012, Malow et al., 1996). However, electrical impulses are delivered in long trains over several seconds and can disrupt function during many different components of a task (stimulus presentation, sentence processing, word retrieval, or word expression). It is therefore difficult at times to interpret ESM results to determine which functions are performed by different cortical regions since the outcome is an all-or-nothing response. In addition, studies have demonstrated that both auditory and visual naming deficits have resulted from resection of sites deemed nonessential for visual naming but essential for auditory descriptive naming using ESM (Hamberger et al., 2005). This finding illustrates a potential limitation of ESM of language.

Administration of an exhaustive battery of language tasks using ESM is often not feasible. ESM is time-consuming and can be limited by poor patient motivation or performance, or by pain caused by stimulation of the trigeminal efferent fibers, preventing comprehensive evaluation. ESM can also provoke after-discharges and seizures, especially during stimulation near a seizure focus, which is typically the region of greatest interest with regard to localizing cortical function for surgery planning. Less invasive and less time intensive language mapping techniques may improve surgical planning and post-operative functional outcomes.

Analysis of recordings of event-related electrocorticographic (ECoG) changes that occur during language tasks provides an alternative method for detecting cortical activation and mapping functional language cortex with high spatial and temporal resolution (Cervenka et al., 2011b, Chang et al., 2010, Crone et al., 1998, Crone et al., 2001, Edwards et al., 2010, Flinker et al., 2011, Jung et al., 2008, Kojima et al., 2012, Mainy et al., 2008, Ritaccio et al., 2010, Sinai et al., 2005a, Tanji et al., 2005, Towle et al., 2008, Wu et al., 2010). Because this is a passive recording technique, ECoG mapping does not increase the risk of seizures or after-discharges and cannot inflict pain. Investigations of changes in ECoG power within the time–frequency domain have revealed that a broadband increase in power in the high gamma (> 60 Hz) frequency range is a reliable marker of cortical activation (Cervenka et al., 2013, Crone et al., 1998). Studies have recently shown improving sensitivity and specificity of ECoG mapping of high gamma activity compared to ESM of motor function (Brunner et al., 2009, Leuthardt et al., 2007) as well as both receptive and expressive components of language (Cervenka et al., 2011b, Kojima et al., 2012, Sinai et al., 2005a, Sinai et al., 2009, Towle et al., 2008), and of auditory perception (Boatman-Reich et al., 2010, Cervenka et al., 2011a, Cervenka et al., 2013). In certain circumstances, ECoG mapping has also been shown to predict post-operative deficits not predicted by ESM (Cervenka et al., 2011b, Kojima et al., 2012).

We studied 16 patients with a total of 933 electrodes implanted over dominant cortex and compared localization of auditory descriptive naming and visual object naming using ECoG mapping of high gamma activity. We hypothesized that sites specific to auditory descriptive naming but not visual object naming as identified by ECoG mapping of high gamma activity would fall within the boundaries of a typical dominant temporal lobectomy (up to 4.5 cm from the anterior temporal tip) or anterior frontal resection (BA 8–11, 46, or 47) sparing Broca's area, primary, and premotor cortices.