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Direct Electrical Stimulation Mapping of Cognitive Functions in the Human Brain Cognitive Neuropsychology ISSN: 0264-3294 (Print) 1464-0627 (Online) Journal homepage: https://www.tandfonline.com/loi/pcgn20 Direct electrical stimulation mapping of cognitive functions in the human brain Bradford Z. Mahon, Michele Miozzo & Webster H. Pilcher To cite this article: Bradford Z. Mahon, Michele Miozzo & Webster H. Pilcher (2019) Direct electrical stimulation mapping of cognitive functions in the human brain, Cognitive Neuropsychology, 36:3-4, 97-102, DOI: 10.1080/02643294.2019.1630375 To link to this article: https://doi.org/10.1080/02643294.2019.1630375 © 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group Published online: 12 Sep 2019. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=pcgn20 COGNITIVE NEUROPSYCHOLOGY 2019, VOL. 36, NOS. 3–4, 97–102 https://doi.org/10.1080/02643294.2019.1630375 INTRODUCTION Direct electrical stimulation mapping of cognitive functions in the human brain Bradford Z. Mahon a,b,c,d,e, Michele Miozzof and Webster H. Pilcherb aDepartment of Psychology, Carnegie Mellon University, Pittsburgh, PA, USA; bDepartment of Neurosurgery, University of Rochester Medical Center, Rochester, NY, USA; cDepartment of Neurology, University of Rochester Medical Center, Rochester, NY, USA; dCarnegie Mellon Neuroscience Institute, Carnegie Mellon University, Pittsburgh, PA, USA; eDepartment of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USA; fDepartment of Psychology, The New School, New York, NY, USA ABSTRACT ARTICLE HISTORY Direct electrical stimulation (DES) is a well-established clinical tool for mapping cognitive functions Received 12 May 2019 while patients are undergoing awake neurosurgery or invasive long-term monitoring to identify Revised 30 May 2019 epileptogenic tissue. Despite the proliferation of a range of invasive and noninvasive methods Accepted 5 June 2019 for mapping sensory, motor and cognitive processes in the human brain, DES remains the KEYWORDS clinical gold standard for establishing the margins of brain tissue that can be safely removed fi Direct electrical stimulation; while avoiding long-term neurological de cits. In parallel, and principally over the last two brain surgery; brain tumour; decades, DES has emerged as a powerful scientific tool for testing hypotheses of brain neural plasticity; cognitive organization and mechanistic hypotheses of cognitive function. DES can cause transient “lesions” models; causal evidence and thus can support causal inferences about the necessity of stimulated brain regions for specific functions, as well as the separability of sensory, motor and cognitive processes. This Special Issue of Cognitive Neuropsychology emphasizes the use of DES as a research tool to advance understanding of normal brain organization and function. Direct electrical stimulation (DES) is a technique that DES has proven to be an indispensible tool for inform- has been in widespread clinical use for over half of a ing the maximal safe resection for tumour or epilepsy century. Clinical applications of DES include real-time surgery—it allows for a tailored resection of pathologi- mapping of sensory, motor and cognitive functions cal tissue while minimizing the likelihood of post-oper- during awake surgery, identifying functional path- ative cognitive impairments (Bloch et al., 2012; Brown ways, quelling epileptiform activity through chroni- et al., 2016; Rech, Herbet, Moritz-Gasser, & Duffau, cally implanted closed loop devices, and reducing 2014; Sanai, Mirzadeh, & Berger, 2008; Santini et al., tremor in motor disorders. There is a longstanding 2012; Satoer et al., 2014; Schucht, Moritz-Gasser, and rich literature using DES in animal models, starting Herbet, Raabe, & Duffau, 2013). A testament to the in the nineteenth century, and running through importance of DES as a clinical tool is the fact that it modern studies that pair DES with neurophysiological has remained the gold standard for mapping func- recordings and in vivo and histological measures of tions in the human brain in a neurosurgical context the effect of electrical current on brain tissues (see for over half a century despite the facts that (i) a review in Mazurek and Schieber, 2019). The particular range of other invasive and non-invasive neuroima- focus of the articles collected together in this Special ging techniques are now available, and (ii) important Issue of Cognitive Neuropsychology is on the use of challenges have been recognized that attend the DES during awake neurosurgery, or through chronic use of the technique (Borchers, Himmelbach, Logothe- implantation of electrodes, to map sensory, motor tis, & Karnath, 2011). and cognitive function in the human brain. The prox- DES is powerful because stimulation of a brain imate goal of the use of DES in those procedures is to region that supports a given cognitive, sensory, inform neurosurgical decisions about what tissue is motor ability can render a patient transiently unable safe to resect from the standpoint of minimizing to perform that ability, evoke a transient sensory post-operative neurologic impairment. In this regard, percept in the absence of a sensory stimulus, a CONTACT Bradford Z. Mahon [email protected] © 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/ 4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way. 98 B. Z. MAHON ET AL. movement in the absence of an intention to move, or is, providing surgeons with real-time feedback in the the experience of an intention to move in the service of intra-operative decisions about the absence of an overt movement (Desmurget et al., margins of tissue that can be safely removed. The 2009); for review and discussion see (Borchers et al., use of DES to advance basic scientific understanding 2011; Desmurget, Song, Mottolese, & Sirigu, 2013). of cognitive brain function and organization will Broadly speaking, there are two types of causal infer- always be constrained by the clinical realities that ences that are derived from observations of how DES motivate the use of the technique in any given disrupts or does not disrupt performance in a given patient (Chiong, Leonard, & Chang, 2017). However, task. First, DES supports real time inferences about within that framework, and as demonstrated by the necessity of a given brain region or pathway for a some of the contributions herein (Chernoff et al., given cognitive function. Second, DES supports causal 2018; Herbet, Moritz Gasser, Lemaitre, Almairac, and inferences about the separability of sensory, motor Duffau (2018); Leonard et al., 2019; Orena et al., and cognitive abilities, and by inference, the separabil- 2019), with appropriate planning and preparation, it ity of representations and computations integral to is possible to interleave into the clinical procedure those abilities. Four of the contributions in this issue causal tests of theories of brain organization and func- emphasize both types of causal inferences through tion (see also, e.g., Chernoff et al., 2018;Duffau & new empirical findings with DES (Chernoff, Sims, Capelle, 2001;Duffau, Gatignol, Denvil, Lopes, & Smith, Pilcher, & Mahon, 2019; Herbet, Moritz-Gasser, Capelle, 2003;Duffau et al., 2002; Garcea et al., 2017). Lemaitre, Almairac, and Duffau (2018); Leonard et al., An important generalization, reviewed in Mazurek 2019; Orena, Caldiroli, Acerbi, Barazzetta, & Papagno, and Schieber (2019), is that using DES to map function 2019). in the brain critically depends on the patient being The modern application of DES for mapping brain able to focus on and be engaged by an appropriate function involves local stimulation of brain tissue with task. The type of task that is selected to map a given direct current in the range of .5–15 milliamps (mA) brain region is influenced by a number of factors, (Kayama, 2012; Sanai et al., 2008; Szelényi et al., 2010). including the purported function of that region, DES can be applied via a hand held bipolar or monopo- results of pre-operative non-invasive mapping (e.g., lar stimulator, or through implanted grids or strips; the fMRI, MEG), and patient-specific factors (e.g., if the former technique is more frequently used during patient is bilingual or monolingual, Benjamin et al., awake craniotomies, while the latter technique is 2017; Fernández-Coello et al., 2013a;Połczyńska, Ben- used in the setting of long-term monitoring and jamin, Japardi, Frew, & Bookheimer, 2016;Połczyńska, extra-operative mapping of the margins separating Japardi, & Bookheimer, 2017). Regardless of the task or epileptogenic from eloquent tissue. The awake craniot- region, however, both patient participation and the omy was the clinical preparation in which DES was clinical team’s ability to “read” the patient’s behaviour developed for use in humans, by pioneers such as in real time are critical. For instance, for motor Wilder Penfield and George Ojemann (Ojemann, mapping, disruptions in voluntary movement are out- 1979, 1981, 1983a, 1983b, 1983c, 1986, 1987, 1988; wardly observable by the clinical team, and thus the Penfield,
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