Does Electrical Stimulation Map Brain Function?

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Background

Since Penfield’s pioneering approach to cortical mapping in epilepsy surgery, electrical stimulation has been almost exclusively used to delineate the so-called “eloquent cortex” prior to surgical resection. Sensory, motor, and language functions are still assessed through behavioral responses to electrical stimuli delivered at the surface of the cerebral cortex.

This tool has allowed clinicians to temporarily and reversibly perturb cortical function, simulating the acute behavioral effects of focal lesions, albeit without the opportunity for recovery or reorganization. In conjunction with studies of the behavioral effects of chronic focal lesions, electrical stimulation has been instrumental in the early development of experimental neurophysiology, and in clinical practice, it has been used to predict neurological outcomes from surgery for tumors, epilepsy and arteriovenous malformations.

However, there has also been a growing appreciation that the neural substrates of cognitive and behavioral processes are not strictly localized and require both serial and parallel coordination of neural activity across widely distributed networks. Indeed, a great deal of data generated by fMRI in cognitive neuroscience during the last three decades has substantiated the involvement of widespread cortical networks during both simple and complex tasks.

What does “functional mapping” mean?
Is it a representational map generated by plotting responses without ensuring actual functional inferences?

The core issue is whether electrical stimulation can adequately apprehend the complex structure behind the function. To answer affirmatively, one can argue that stimulation of primary cortices reveals a topography of sensory or motor representations, and that the functional significance of this topography is attested by the observation of post-operative sensory or motor impairments after resecting these areas. On the other hand, one can argue that stimulation of premotor or cingulate motor cortex induces equally dramatic motor effects, of basal temporal or lateral occipital cortex impairs face recognition, of entorhinal cortex causes deja-vu, etc., but that no permanent deficit will typically follow their resection.

The clinical significance of language functional mapping by electrical stimulation is an even more challenging issue. Whereas stimulation of primary or unimodal associative sensory areas may produce positive symptoms (e.g. hallucinations) in their respective modality, stimulation of language areas typically provokes global or selective inactivation of speech, reading, writing, and of other language processes. The spatial distribution of the cortical areas where these inactivation effects are observed extends far beyond the limits of the classical Broca-Wernicke model of speech production with large inter-individual variability. In epilepsy surgery, the predictive value of stimulation-induced effects on the functional outcome has never been rigorously validated. Two types of observations deserve reflection. Electrode placement and size, as well as stimulation parameters, are completely different in subdural ECoG grid (SDG) vs SEEG (depth electrodes) recordings. The probability of producing language impairment through electrical stimulation of the cortex is much higher in SDG than in SEEG. But stimulus intensity can be superior by a factor of ten. SEEG stimulation seems to be more effective in the white matter underlying language areas. In tumor surgery, resection of the “eloquent” cortex without long-term post-operative deficit has been documented. Moreover, a number of reports in the past decade based on stimulation of white matter tracts have emphasized the importance of taking a network approach for a presurgical language evaluation.

The aim of this Research Topic is to examine the role and significance of electrical stimulation in evaluating the “functions” subserved by cerebral cortex areas being considered for resection during neurosurgical procedures.

Theoretical, experimental, and computational modeling studies of stimulation are included in the Research Topic. Methodological strategies that reflect on the practical use of pre-operative or intra-operative functional mapping are also included. Interpretation of clinical and neuropsychological data gathered in the course of SDG and/or SEEG investigations is also a focus for this topic. Comparison of electrical functional mapping with fMRI, MEG or intracerebral physiological recordings of task-related activities are also within scope, as well as studies with any of these modalities in relation to surgical outcome. Finally, new methods for a more appropriate evaluation of cognitive/behavioural processes prior to surgery will be most welcomed.

Keywords: Brain functional mapping, cerebral cortex areas, cognition, language, ECoG grid (SDG), SEEG, brain stimulation

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