Negative motor responses to direct electrical stimulation: Behavioral assessment hides different effects on muscles

A negative motor response (NMR) is defined as the inability to continue voluntary movements without losing consciousness when direct electrical stimulation (DES) is applied during awake neurosurgery. While visual inspection is most commonly used to define an NMR, the actual effect of stimulation on muscle activity has been neglected by recent neurosurgical literature. We show that behavioral assessment of NMRs hides different site-dependent effects on muscles as revealed by electromyography (EMG), describing ten cases of brain tumor patients undergoing awake neurosurgery while performing a hand-object manipulation task. DES-induced NMRs were assessed behaviorally and related to the underlying electromyographic recording. Quantitative analysis of motor unit recruitment and regularity between phasic muscle contractions was computed. We show that similar NMRs classified based on behavioral criteria can be associated with suppression, increased recruitment or mixed effects on ongoing hand muscles. In some cases, suppression of hand muscle activity is associated with involuntary recruitment of muscles not involved in the task. Interestingly, stimulation of behaviorally defined "negative areas" across the frontal and parietal lobes elicits different electromyographic patterns, depending on the stimulation site. This study provides novel preliminary background as to the heterogeneous profile of muscle activity during NMRs. In fact, EMG monitoring paired with behavioral assessment can distinguish between NMRs that, despite similarity on behavioral inspection, are different in their related EMG, possibly underlying different neural substrates. The identification of different circuits hidden in similar NMRs may become relevant when planning the extension of resection.