Peri- and intraoperative cognitive and language assessment for surgical resection in brain eloquent structures

Neurochirurgie 63 (2017) 135–141

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Original article

Peri- and intraoperative cognitive and language assessment for surgical resection in brain eloquent structures G. Herbet a,∗,b , O. Rigaux-Viodé c,d , S. Moritz-Gasser a,b a

Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University medical center, 80, avenue Augustin Fliche, 34295 Montpellier, France Institute for Neuroscience of Montpellier, Inserm U-1051, Saint-Eloi Hospital, 80, rue Augustin-Fliche, 34091 Montpellier cedex 5, France Department of Neurosurgery, Saint-Anne Hospital Center, 1, rue Cabanis, 75014 Paris, France d University Paris-Descartes, 12, rue de l’École de Médecine, 75006 Paris, France b c

a r t i c l e

i n f o

Article history: Received 12 April 2016 Accepted 17 October 2016 Available online 12 May 2017 Keywords: Neuropsychological care Neuropsychological assessment Intraoperative cognitive mapping Diffuse low-grade glioma Neuropsychological rehabilitation

a b s t r a c t Neuropsychological care of patients suffering from an infiltrative glioma and candidates for a neurosurgery under awake condition with intraoperative functional mapping is a critical and mandatory stage in therapeutic management. It enables to estimate the functional impact of the tumor and, consequently, the efficacy of functional reorganization typically observed in these patients, not only to better predict surgery outcomes and select appropriate tasks for intraoperative functional mapping, but also to plan efficient and individualized postoperative cognitive rehabilitation strategies. Neuropsychological care management also enables patients to benefit from a solid psychological preparation both to the surgery and its associated transitory functional consequences, as well as provide a personalized psychological and emotional long-term support. Based on their solid experience in the peri-operative care of diffuse low-grade glioma patients, the authors thoroughly describe the different stages of neuropsychological management. Cognitive, emotional and language assessments typically used by the authors around and during surgery are reported, and different possible avenues of improvement are further discussed. © 2017 Elsevier Masson SAS. All rights reserved.

1. Introduction

2. Rationale of a perioperative functional assessment

Diffuse low-grade glioma (DLGG) is a slow-growing, primary brain tumor mainly occurring in young adults, and most often diagnosed following an inaugural seizure [1]. Although its incidental detection is currently increasing notably due to a broader access to neuroimaging [2]. Given its acknowledged clinical benefits (i.e. increase of overall median survival, time to anaplastic transformation while preserving or even improving quality of life), surgical resection with intraoperative functional monitoring under awake conditions is now recognized as the first-line treatment in the care of DLGG patients [3,4]. However, for this oncofunctional treatment to be truly effective it has to be accompanied by precise and specific neuropsychological care, which has to be administered by a trained neuropsychologist and/or speech therapist, for a number of reasons. In this chapter, we describe the different steps of the neuropsychological care of DLGG patients. We begin by describing peri-operative cognitive and language assessments in some details. Later, we touch upon the issue of intraoperative cognitive tasks.

First, contrary to what it is sometimes suggested, DLGG patients frequently suffer from neuropsychological disturbances [5], even in the case of incidental discovery [6]. This decrease in cognitive functioning generally concerns attention resources, memory, information processing speed, and more complex cognitive control functions such as dual tasking—all together impacting the quality of life [7]. The observed impairments can be partly explained by a number of socio-demographical factors, such as educational level, and are often exacerbated by anti-epileptic drug therapies [3,8], by fatigue which is recurrent in these patients [9], or by well-comprehensible psychological-related reasons. However, their very origins prior to any oncological/surgical treatment are above all pathophysiological (DLGG) location and size, infiltration or not of white matter pathways [10]. Although DLGG can induce a long-term neuroplasticity, this remains nevertheless limited, especially for certain brain structures (e.g. low plasticity of white matter tracts) [11,12]. Detailed preoperative neuropsychological information is therefore crucial to assess individual limitation in neuroplasticity potential and to subsequently predict postoperative surgical outcomes more precisely. Second, as awake surgery is a highly unusual clinical situation, patients must be well prepared on both the psychological

∗ Corresponding author. E-mail address: [email protected] (G. Herbet). http://dx.doi.org/10.1016/j.neuchi.2016.10.011 0028-3770/© 2017 Elsevier Masson SAS. All rights reserved.

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and neuropsychological levels. This optimal preparation entails, not only a very detailed description of the procedure but also a thorough explanation regarding the administration of the cognitive/language/neurological tests that will be performed during surgery (well-trained patients permit to strongly increase the objectivity of the intraoperative assessment). It also allows patients to be prepared for the immediate postoperative phase. Based on interviews of patients who had undergone awake surgery for DLGG (personal experience), awake surgery itself does not generally constitute a traumatic experience for the patient; the postoperative period is clearly more distressing due to transient impairments (i.e. complete aphasia, akinetic mutism, hemiplegia, spatial neglect, behavioral disinhibition, etc.). This experience can be quite profound for both the patients and their families. It has to be anticipated and clearly explain to patients. Third, neuropsychological care enables to select appropriate and individualized tasks for intraoperative mapping. Although a set of cognitive/language tasks is typically used depending on cerebral networks damaged by the tumor (see below), the preoperative neuropsychological assessment—allowing to determine which functions are impaired by the tumor and which are the patient’s cognitive expertise—permits, if required, to tailor the tasks that will be used during intraoperative functional mapping. Fourth, the immediate postoperative neuropsychological/language assessment in conjunction with the preoperative assessment gives a complete picture of surgery’s functional consequences. This critical stage will allow proposing an individualized neuropsychological rehabilitation strategy. We know that early, intensive and individualized care is very beneficial and required to reach or at least to tend towards a full recovery. Last, neuropsychological and psychological follow-up allows quantifying the recovery, reorienting cognitive/language rehabilitation if required, and providing psychological support. 3. Peri-operative cognitive assessments The neuropsychological management of DLGG patients should be highly controlled, and structured following the same temporal organization (See Fig. 1). Cognitive and language assessments are administered three times during the peri-operative period: The week before surgery, three to five days after surgery and three months after. It is worth noting here that a language or cognitive rehabilitation is always administered to the patients during this 3month period (sometimes, an orthoptic rehabilitation is performed when disturbances of visual or visuospatial processes are observed and a physiological rehabilitation is performed when sensorimotor disturbances are observed). Of course, the choice of cognitive and language tasks is individually-based, depending on the therapist and the patient. The matter here is not to impose an assessment protocol but rather to describe a well-tried standard examination (experienced with more than 500 patients). The proposed assessment takes into consideration critical parameters and constraints: • in our centers, patients come from all over the country, Europe and even parts of the world. As a result, in some cases, it not always possible to see the patients several times before or after surgery. The assessment must then be at the same time sensitive, relevant and comprehensive but not too long; • moreover, this is justified by the fact that, beyond the possible functional consequences of the lesion/resection, DLGG patients generally suffer from fatigue (inducing reduced concentration and motivation) and take anti-epileptic drugs (inducing concentration disturbances, fatigue and slowdown). If the testing is too

Table 1 Peri-operative cognitive assessment. Cognitive assessment other than language Pre- and 3-month postoperative cognitive assessment

General Complaints inventory Subjective reports/Questionnaires Handedness Working Memory Digit span test [39] Information Processing speed Digit Symbol (WAIS-IV) [40] Verbal and nonverbal long-term memory RL/RI 16, Rey’s Figure [41] Praxis Motor, ideomotor, reflexive, constructive Visual gnosis V.O.S.P [42] Somatognosis and body Schema Visuospatial cognition The Bells test, line bisection task [43] Attention T.E.A or D2, PASAT, Baddeley’s Dual task [44] Executive functions Motor and verbal inhibition (go/no go) [45,46], shifting (TMT), visuospatial planning (Rey’s Figure) [47] and auto-generation (Fluency task) Social cognition and emotion Mentalizing (Comic strips task, Read the Mind in the Eyes Task), basic emotion recognition (Ekman’s face) and other personal materials [48] When possible: general intellectual functioning Verbal Comprehension, perceptive organization, working memory, processing speed (WAIS-IV)

Immediate postoperative cognitive assessment (3/5 days after) Yes No No Yes Yes No Yes Yes Yes Yes No Yes

Only the Read the Mind in the Eyes task No

Language assessment General Complaints inventory Subjective reports/Questionnaires Fluency/informativity Used Tasks Timed naming task [49] Fluency Task Timed semantic association task [50] Timed reading task Repetition task Lexicality judgment Writing Comprehension (Token test) [51] Metaphoric/implicit language Prosody

Yes No Yes Yes Yes Yes Yes Yes No Yes Yes No No

Note that other more specific tasks are sometimes used such as metacognition or moral cognition tasks. Note also that detailed discussion of the presented tests is in the main body of test.

long, the results will be biased and will not reflect the patient’s actual cognitive status; • most of the assessment must be feasible a few days following surgery; • the same assessment has to be equally valid for all patients; • we will describe the peri-operative cognitive and language assessment typically administrated to the patients. A complete overview of the core assessment is provided in Table 1. 3.1. Peri-operative assessment: cognitive functions other than language A comprehensive set of cognitive and emotional tasks is always proposed the week before, three to five days after and three months after surgery. This core assessment includes a measure

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Fig. 1. Time course of neuropsychological care.

of information processing speed, short term and working memory (including both the verbal and the non verbal modality). The different executive sub-functions (i.e. cognitive flexibility, inhibition and auto-generation) are also assessed. Visual, visuospatial and motor cognitions are also reviewed. Importantly, social cognition, including emotion recognition and mentalizing is also subject to a thorough examination. Depending of the lesion location other aspects must be assessed such as somatognosia and body scheme. During preoperative and the three-month postoperative assessment verbal and non-verbal long-term memory is also routinely assessed. If possible, other tasks regarding global intellectual functioning and the different aspects of attention are performed. Depending of the tumor location and the patient’s complaint, other specific tasks may be proposed to have convergent cognitive measures.

4. Intra-operative assessments Here are described the different tasks used during surgical resection with intraoperative functional monitoring under awake conditions. A complete overview is provided in Table 2. 4.1. Cognitive/motor tasks 4.1.1. Motor cognition Voluntary movement (i.e. the consequence of internal/endogenous activity) engages a set of highly sophisticated

Table 2 Intraoperative tasks. Tasks

3.2. Peri-operative assessment: language functions The same battery of language testing is always used before, immediately after and three months after surgery, whatever the location of the DLGG. This gold standard assessment is constituted by an evaluation of the level of fluency and informativity of spontaneous speech; a timed naming task (response times are registered for each passed item), which consists of naming black and white pictures; a fluency task (semantic and phonological), which consists of producing the highest number of words belonging to a given sematic category or beginning by a given letter during two minutes; a timed nonverbal association task (Pyramids and Palm Trees Test), which consist of matching two semantically related pictures; a timed reading task, in which the patient is asked to read aloud a text and a list of regular, irregular and pseudo words (See Table 1). Depending on the tumor location, others tasks may be added to this basic assessment such as, for example, a task assessing the comprehension of metaphoric language.

Routinely used Counting task Naming task Semantic association Task Double task (motor movement plus naming) Double task (motor movement plus semantic association) Mentalizing task Depending on tumor location Line bisection task (visuospatial cognition) Visual fields Reading aloud task Repetition task Bi-manual movements Motor or ideomotor praxis Coordinated movements of the leg and the arm n-back task Simple calculation task a

Left hemisphere

Right hemisphere

Yes Yes Yes Yes

Yes Yes Yes Yes

No

Yes

No

Yes

No

Yes

Yes Yes Yes Yes Yes Yes

Yes No* No* Yes Yes Yes

Yes Yes

Yes Noa

Can be used if the patient is ambidextrous or left-handed.

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processes grouped under the term of motor cognition (i.e. intention to act, motor planning, motor initiation, action control, etc.). Impairment of motor cognition can lead to a variety of disabling disorders, such as for example disturbance of bimanual coordination or ideomotor motor apraxia. A basic way to intra-operatively monitor all aspects of voluntary movement is to ask the patient to perform a simple double motor task engaging the upper limb: lower the arm and open the hand, then raise the arm and close the hand (the lower limb may be also concerned or both at the same time). In addition to control the velocity and the accuracy of the movement during all the surgery, this task enables to map under stimulation crucial areas for motor cognition [13]. Depending on the structures being stimulated, a wide range of manifestations can be observed. For example, stimulation of the supplementary motor area can lead to motor initiation disturbances. Other motor tasks can be performed to map more specific motor abilities. Regularly, we ask the patients to make coordinated movements with both hands [14,15]—an ability especially crucial for certain professions (e.g. manual work, musician). It is also important to ask the patient to perform more complex movements to assess fine-grained motor abilities such as drumming, or to perform reflexive praxis (e.g. imitation of meaningless movements) to evaluate movement planning. Note that, in certain centers, a physiotherapist is present in the operating theater in order to analyze the characteristics of induced movements during the intraoperative evaluation of motor cognition. 4.1.2. Spatial cognition Unilateral spatial neglect is a debilitating condition characterized by a failure to explore and allocate attention in the space contralateral to the damaged hemisphere [16]. It occurs mainly after a right lesion (especially when the lesion involves the right parietal lobe or the temporo-parietal lobes). This cognitive impairment has a major impact on quality of life by depriving the patient to resume a normal social and professional life. A classical test to evaluate spatial neglect is the bisection line task [17]. For surgery, we have adapted this task in a touch-screen environment. The patient is asked to separate a line into two identical segments (i.e. find the middle of the line). The length of the line is 18 centimeters. If, during the time of stimulation, a significant rightward deviation is observed (typically 7 millimeters or slightly more if the patient present with a behavioral variability), the brain areas under scrutiny is considered as eloquent for visuospatial cognition. This task is especially useful to map the inferior and the superior parietal lobule and, most importantly, the dorsal white matter connectivity (i.e. especially the layer II of the superior longitudinal fasciculus) [18,19]. Using this method, in our experience, none of our patients have presented a long-term spatial neglect although approximately half of the patients with a right lesion experience a transitory neglect in the immediate postoperative phase [20]. 4.1.3. Social cognition Social cognition refers to the set of processes involved in the understanding of interpersonal relationships [21]. Impairment of social cognition in general, and of mentalizing in particular (i.e. the ability to impute mental states to others), is a characteristic feature of numerous brain conditions including psychopathologies such as autism spectrum disorders or neurodegenerative processes such as frontotemporal dementia [22]. Patients with social cognition disorders have difficulties to understand their environment leading to abnormal behaviors and lack of social flexibility. To avoid long-term postoperative social cognition impairments, we use an adapted version of a well-used mentalizing task (i.e. the Read the Mind in the Eyes Task) [23]. The original version of this behavioral task consists of the presentation of 36 photographs

depicting the eye region of human faces. For each of them four affective states are suggested and participants are asked to select the one that best describes what the person on the photograph is currently feeling or thinking. We have indeed previously shown that patients with a resection of the pars opercularis of the right inferior frontal gyrus did not completely recover after surgery [10,24], justifying the use of a new intraoperative task. This task has proven to be especially useful to functionally map not only the pars opercularis and the pars triangularis and their underlying neural connections [25], but also the posterior part of the dorsolateral prefrontal cortex and its underlying connectivity (i.e. the superior longitudinal fasciculus and the inferior fronto-occipital fasciculus) (Submitted work). 4.1.4. Visual processes Patients with a large visual field defect, such as lateral homonymous hemianopia, have generally a poor functional outcome. In many countries, driving is formally prohibited and a lot of activities such as reading become arduous. To map visual connectivity and avoid the occurrence of long-term postoperative visual field defects, we use a simple protocol allowing to assess visual fields during surgery [26]. Specifically, with the vision being fixed at the center of the screen, patients are asked to name successively two pictures disposed in the two opposite quadrants knowing that it is absolutely crucial to preserve the inferior quadrant (the superior being compensable). The position of the pictures is determined by the laterality of the lesion. Although direct electrical stimulation of visual pathways, especially the optic radiations, generally evokes a range a phenomena subjectively described by the patient himself (blurred vision, impression of shadow, phosphenes, visual hallucinations such as zoopsia or metamorphopsia), the described task allows to have a more objective confirmation of the transitory visual disturbance induced (i.e. the patient cannot name the picture presented in the inferior quadrant contralateral to the lesion). Some indicators are also important to take into consideration during the assessment of visual fields, most notably the amplitude of visual saccades or the possible increase of naming response time in the visual field under scrutiny. It is also very important to regularly assess manually the extent of the visual field of the patient. 4.1.5. High-order visual processes The inferolateral occipito-temporal cortex is reputed to broadcast critical information in the service of object recognition. Damage to this neural system may lead to visual agnosia. A simple way to map these high-order visual processes is to use a picture naming task. If a disturbance of object recognition is induced during electrostimulation, the patient generally commits a nonsemantically related ‘visual’ paraphasia. Our group has previously shown that electrostimulation of the right inferior longitudinal fasciculus, connecting the occipital cortex with the temporal pole, can lead to such impairments [27,28]. 4.1.6. Dual-tasking and multi-tasking Numerous activities in daily life necessitate to process different matters at the same time. This crucial multitasking ability requires maintaining in working memory several task goals to be performed and concurrently allocating attention among them. During surgery, this higher capacity can be assessed by asking the patient to perform simultaneously a regular movement of the upper limb (see section 4.1.1) and a naming task or a semantic association task. A multitasking disturbance is observed when the patient is no longer able to perform both tasks at the same time while the realization of each task separately remains possible. This impairment, to a lesser extent, may be manifested in a temporary desynchronization/lack of coordination between the two tasks.

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4.2. Language tasks To map language processes, the use of a naming task remains the gold standard. This task, which is easy to implement during surgery and especially adapted to patient positioning constraints, as well as is very sensitive to all levels of processing. During electrostimulation, different kinds of impairments may be observed: speech arrest, dysarthria (disturbance of motor programming), anomia (disturbance of lexical retrieval: the patient is unable to name the object), phonological paraphasia (disturbance of phonological encoding: production of a word with phonological deviations, e.g. phelephant for elephant), semantic paraphasia (disturbance of semantic processing, production of a word semantically related to the target word, e.g. cow for horse) or perseveration (disturbance of inhibitory control mechanisms, repetition of a prior word in front of a new picture) [29]. Beyond classical language-related cortical areas, the naming task enables to map the main associative connectivities (i.e. the arcuate fasciculus for phonological processes, the lateral superior longitudinal fasciculus for articulatory processes, the inferior fronto-occipital fasciculus for semantic control processes and the inferior longitudinal fasciculus for lexical retrieval) and certain intralobar tracts, such as the frontal aslant tract (speech initiation and control) [30,31]. To intraoperatively assess the non verbal semantic system (the naming tasks enables only to assess verbal semantics), we also routinely use a semantic association task (i.e. the Pyramids and Palm Trees Test). This task consists of 52 black and white drawn pictures. For each target picture, two new pictures are proposed and the patient is asked to match one of both with the target one according to the semantic link, by pointing it out. We have previously shown that this task is useful to map and preserve the direct ventral connectivity, especially the inferior fronto-occipital fasciculus in the left hemisphere [32] but also in the right hemisphere [33]. When the tumor concerns the left occipito-temporal cortex, especially the visual word forms area and its underlying white matter connectivity, it is necessary to map the different sub processes involved in reading aloud. To this end, we typically use a reading task in which the patient is asked to read aloud different word categories, including regular and irregular words, and pseudo-words [34]. Depending on the structure stimulated, different neuropsychological disturbances can be observed. For example, stimulation of the anterior part of the visual word forms area induces addressed phonology disturbances (irregular word reading) while stimulation of the posterior segment of the superior longitudinal fasciculus induces both addressed and assembled phonology disturbances (irregular words and pseudo words reading). Finally, to map brain areas involved in the motor implementation of automatic speech production, we routinely use a counting task consisting in counting aloud from 1 to 10 in loop. 4.3. Other cognitive tasks Patients may have a strong expertise in some cognitive domains due to their occupation or their hobbies (numerical cognition in a mathematician expert, working memory in a management assistant). In such cases, we can implement some specific tests to ensure the patient that he/she will recover a normal professional life after surgery. For example, we regularly use a two-back task to assess working memory. This task consists of naming the picture viewed two trials before. For high-level patients, we can exceptionally increase cognitive load by asking the patient to name the picture viewed three trials before. On several occasions, we have also used mathematical cognition tasks to assess basic mathematical operations. This is useful when the lesion is located in the left parietal lobules. For example, we can ask the patient to mentally resolve simple operations such as 8 + 11

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or 12 − 4. These operations can be visually displayed on a computer screen. 4.4. Should we introduce other tasks? An issue frequently raised by our colleagues concerns the use of other cognitive/language tasks for the intraoperative mapping such as more fine-grained linguistic or memory tasks, or specific executive function tasks. It is a fair question. However, in our opinion, deciding to implement new tasks in standard practice involves several considerations: • the cognitive tasks previously described appears to be sufficient to map both the main white matter connectivities and the cortical epicenters which are reluctant to brain plasticity (see [12] for a probabilistic atlas of neuroplasticity potential in glioma patients); • the tasks used must be necessary simple and easily workable given the constraints inherent to the electrostimulation procedure (stimulation duration: 4 second maximum), clinical contexts (intraoperative mapping cannot be too long), and surgery theater constraints (patient position); • in connection with this, high-level functions such as for example certain executive functions particularly distributed at the anatomical scale are probably very difficult to map under stimulation (simultaneous contribution of multiple networks); • the best onco-functional balance must be found: the first goal towards the surgery is to optimize the quality of the resection while preserving quality of life. Adding too many tasks might eventually affect the effectiveness of surgery. In our opinion, supplying an objective answer to this question necessitates longitudinally studying (i.e. before and after the surgery) patients’ cognitive and language performances on a variety of behavioral paradigms. If patients do not recover sufficiently and are impeded in their daily life functioning, it seems reasonable to think to the implementation of new well-controlled tasks. However, before doing this, we have to comprehend the pathophysiological mechanisms of the lack of recovery. Indeed, a number of factors can explain a lack of recovery after surgery such as the degree of infiltration of white matter connectivity [8,35,36], the preoperative functional status, and the inter-individual variability in the neuroplasticity potential, the socio-educational level, and probably the patients’ personality. Similarly, it is not uncommon to see certain patients developing behavioral abnormalities, which could be termed personal identity disorders. Although their occurrence remains rather low, they may severely affect the patient’s quality of life and those of their family. These behavioral abnormalities are however difficult to anticipate as they can manifest in some patients but not in others–other things being equal. As Minsky had identified it in 1931 [37], changes in behaviors and identity seem to be related to the premorbid personality. Surgery appears to induce an exaggerated/exacerbated version of the preoperative ego in certain patients. In contrast, we have observed that patients with certain personality types/traits (i.e. schizotypal traits, neuroticism) have an increased probability to show more pronounced postoperative decline. On the whole, these clinical observations suggest that a better psychological characterization of patients before surgery may help in anticipating postoperative behavioral abnormalities and, subsequently, may aid in deciding the prescription of postoperative behavioral therapy. 5. Conclusion Neuropsychological perioperative cares are crucial stages in the management of DLGG patients. The neuropsychologist and the

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speech therapist have an essential role to play in the general medical management. They establish a real therapeutic alliance with the patient, which will extent in time, as DLGG is a chronic disease and the patients are regularly followed-up, at least in our centers. It is indeed useful to assess periodically cognitive functioning and some patients clearly require psychological back-up. Institutions and neurosurgeons should imperatively pay more attention to these aspects of management, which are often neglected or underestimated in clinical practice. If the neuropsychological management, along the main lines of that described in this chapter, appears to be now sufficient to ensure the patients the resumption of a relatively normal socioprofessional life in the months following surgery, some challenges still remain. In fact, all patients do not recover all aspects of cognition as regards emotion/affective functions. We absolutely need to understand the reasons governing this lack of recovery, which may be not completely related to the surgical procedure itself by developing more studies assessing the cognitive and emotional processes longitudinally (i.e. before and after surgery) including a wide-range of behavioral tasks on large samples. These types of studies to date continue to be relatively scarce as recently reported by Saoter et al. [38]. On the basis of these future results, it will be possible to identify which aspects of cognition do not fully recover despite early and intensive postoperative cognitive rehabilitation, and subsequently construct new and adapted intraoperative protocols. As a final note, it seems to be of primary importance to develop, in the future, more studies dedicated to the effectiveness of neuropsychological rehabilitation in the context of DLGG surgery. Although we know that cognitive and language rehabilitation is essential to pave the way towards a satisfactory level of recovery, controlled studies demonstrating the merits of this approach are lacking. The results of these studies could provide better guidance for postoperative management. Disclosure of interest The authors declare that they have no competing interest. References [1] Pallud J, Audureau E, Blonski M, Sanai N, Bauchet L, Fontaine D, et al. Epileptic seizures in diffuse low-grade gliomas in adults. Brain 2014;137(2):449–62. [2] Pallud J, Fontaine D, Duffau H, Mandonnet E, Sanai N, Taillandier L, et al. Natural history of incidental World Health Organization grade II gliomas. Ann Neurol 2010;68(5):727–33. [3] De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a metaanalysis. J Clin Oncol 2012;30(20):2559–65. [4] Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frenay M, et al. Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force. Eur J Neurol 2010;17(9):1124–33. [5] Taphoorn MJ, Klein M. Cognitive deficits in adult patients with brain tumours. Lancet Neurol 2004;3(3):159–68. [6] Cochereau J, Herbet G, Duffau H. Patients with incidental WHO grade II glioma frequently suffer from neuropsychological disturbances. Acta Neurochir 2016;158(2):305–12. [7] Heimans JJ, Taphoorn MJ. Impact of brain tumour treatment on quality of life. J Neurol 2002;249(8):955–60. [8] Park S-P, Kwon S-H. Cognitive Effects of Antiepileptic Drugs. J Clin Neurol (Seoul Korea) 2008;4(3):99–106. [9] Struik K, Klein M, Heimans JJ, Gielissen MF, Bleijenberg G, Taphoorn MJ, et al. Fatigue in low-grade glioma. J Neurooncol 2009;92(1):73–8. [10] Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, Menjot de Champfleur N, Duffau H. Inferring a dual-stream model of mentalizing from associative white matter fibres disconnection. Brain 2014;137(Pt 3):944–59. [11] Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H. Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain”. Neuroimage 2011;56(3):992–1000. [12] Herbet G, Maheu M, Costi E, Lafargue G, Duffau H. Mapping neuroplastic potential in brain-damaged patients. Brain 2016;139(Pt 3):829–44.

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