Skip to main content
SpringerLink
Log in

Intraoperative mapping and preservation of executive functions in awake craniotomy: a systematic review

  • Review Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Awake craniotomy (AC) allows intraoperative brain mapping (ioBM) for maximum lesion resection while monitoring and preserving neurological function. Conventionally, language, visuospatial assessment, and motor functions are mapped, while the assessment of executive functions (EF) is uncommon. Impaired EF may lead to occupational, personal, and social limitations, thus, a compromised quality of life. A comprehensive literature search was conducted through Scopus, Medline, and Cochrane Library using a pre-defined search strategy. Articles were selected after duplicate removal, initial screening, and full-text assessment. The demographic details, ioBM techniques, intraoperative tasks, and their assessments, the extent of resection (EOR), post-op EF and neurocognitive status, and feasibility and potential adverse effects of the procedure were reviewed. The correlations of tumor locations with intraoperative EF deficits were also assessed. A total of 13 studies with intraoperative EF assessment of 351 patients were reviewed. Awake-asleep-awake protocol was most commonly used. Most studies performed ioBM using bipolar stimulation, with a frequency of 60 Hz, pulse durations ranging 1–2 ms, and intensity ranging 2–6 mA. Cognitive function was monitored with the Stroop task, spatial-2-back test, line-bisection test, trail-making-task, and digit-span tests. All studies reported similar or better EOR in patients with ioBM for EF. When comparing the neuropsychological outcomes of patients with ioBM of EF to those without it, all studies reported significantly better EF preservation in ioBM groups. Most authors reported EF mapping as a feasible tool to obtain satisfactory outcomes. Adverse effects included intraoperative seizures which were easily controlled. AC with ioBM of EF is a safe, effective, and feasible technique that allows satisfactory EOR and improved neurocognitive outcomes with minimal adverse effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data Availability

As this is a review of current literature, the associated data can be found in the referenced studies.

References

  1. Dilmen OK, Akcil EF, Oguz A, Vehid H, Tunali Y (2017) Comparison of conscious sedation and asleep-awake-asleep techniques for awake craniotomy. J Clin Neurosci 35:30–34. https://doi.org/10.1016/j.jocn.2016.10.007

    Article  PubMed  Google Scholar 

  2. Hansen E, Seemann M, Zech N, Doenitz C, Luerding R, Brawanski A (2013) Awake craniotomies without any sedation: the awake-awake-awake technique. Acta Neurochir (Wien) 155(8):1417–1424. https://doi.org/10.1007/s00701-013-1801-2

    Article  PubMed  Google Scholar 

  3. Zhang K, Gelb AW, Zhang K, Gelb AW (2018) Awake craniotomy: indications, benefits, and techniques. Colomb J Anestesiol 46:46–51. https://doi.org/10.1097/cj9.0000000000000045

    Article  Google Scholar 

  4. Brown T, Shah AH, Bregy A et al (2013) Awake craniotomy for brain tumor resection: the rule rather than the exception? J Neurosurg Anesthesiol 25(3):240–247. https://doi.org/10.1097/ANA.0b013e318290c230

    Article  PubMed  Google Scholar 

  5. Hall S, Kabwama S, Sadek AR et al (2021) Awake craniotomy for tumour resection: the safety and feasibility of a simple technique. Interdiscip Neurosurg 24:101070. https://doi.org/10.1016/j.inat.2020.101070

    Article  Google Scholar 

  6. Ruis C (2018) Monitoring cognition during awake brain surgery in adults: a systematic review. J Clin Exp Neuropsychol 40(10):1081–1104. https://doi.org/10.1080/13803395.2018.1469602

    Article  PubMed  Google Scholar 

  7. Koziol LF, Lutz JT (2013) From movement to thought: the development of executive function. Appl Neuropsychol Child 2(2):104–115. https://doi.org/10.1080/21622965.2013.748386

    Article  PubMed  Google Scholar 

  8. Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cognit Psychol 41(1):49–100. https://doi.org/10.1006/cogp.1999.0734

    Article  CAS  PubMed  Google Scholar 

  9. Goldstein S, Naglieri JA, Princiotta D, Otero TM (2014) Introduction: a history of executive functioning as a theoretical and clinical construct. In: Goldstein S, Naglieri JA, eds. Handbook of executive functioning. Springer; 3–12. https://doi.org/10.1007/978-1-4614-8106-5_1

  10. Cristofori I, Cohen-Zimerman S, Grafman J (2019) Chapter 11 - Executive functions. In: D’Esposito M, Grafman JH, eds. Handbook of clinical neurology. Vol 163. The Frontal Lobes. Elsevier 197–219. https://doi.org/10.1016/B978-0-12-804281-6.00011-2

  11. Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. https://doi.org/10.1146/annurev-psych-113011-143750

    Article  PubMed  Google Scholar 

  12. Aaronson NK, Taphoorn MJB, Heimans JJ et al (2011) Compromised health-related quality of life in patients with low-grade glioma. J Clin Oncol Off J Am Soc Clin Oncol 29(33):4430–4435. https://doi.org/10.1200/JCO.2011.35.5750

    Article  Google Scholar 

  13. Moffitt TE, Arseneault L, Belsky D et al (2011) A gradient of childhood self-control predicts health, wealth, and public safety. Proc Natl Acad Sci U S A 108(7):2693–2698. https://doi.org/10.1073/pnas.1010076108

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lezak MD (1982) The problem of assessing executive functions. Int J Psychol 17(1–4):281–297. https://doi.org/10.1080/00207598208247445

    Article  Google Scholar 

  15. Nowrangi MA, Lyketsos C, Rao V, Munro CA (2014) Systematic review of neuroimaging correlates of executive functioning: converging evidence from different clinical populations. J Neuropsychiatry Clin Neurosci 26(2):114–125. https://doi.org/10.1176/appi.neuropsych.12070176

    Article  PubMed  PubMed Central  Google Scholar 

  16. Mandonnet E, Winkler PA, Duffau H (2010) Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir (Wien) 152(2):185–193. https://doi.org/10.1007/s00701-009-0469-0

    Article  PubMed  Google Scholar 

  17. Landers MJF, Sitskoorn MM, Rutten GJM, Mandonnet E, De Baene W (2022) A systematic review of the use of subcortical intraoperative electrical stimulation mapping for monitoring of executive deficits and neglect: what is the evidence so far? Acta Neurochir (Wien) 164(1):177–191. https://doi.org/10.1007/s00701-021-05012-w

    Article  PubMed  Google Scholar 

  18. Prat-Acín R, Galeano-Senabre I, López-Ruiz P, Ayuso-Sacido A, Espert-Tortajada R (2021) Intraoperative brain mapping of language, cognitive functions, and social cognition in awake surgery of low-grade gliomas located in the right non-dominant hemisphere. Clin Neurol Neurosurg 200. https://doi.org/10.1016/j.clineuro.2020.106363

  19. Prat-Acín R, Galeano-Senabre I, López-Ruiz P, García-Sánchez D, Ayuso-Sacido A, Espert-Tortajada R (2021) Intraoperative brain mapping during awake surgery in symptomatic supratentorial cavernomas. Neurocirugia 32(5):217–223. https://doi.org/10.1016/j.neucir.2020.07.004

    Article  Google Scholar 

  20. Nakada M, Kinoshita M, Nakajima R, Shinohara H (2017) The function of right frontal lobe and awake surgery. Jpn J Neurosurg 26(9):657–667. https://doi.org/10.7887/jcns.26.657

    Article  Google Scholar 

  21. Mandonnet E, Vincent M, Valero-Cabré A et al (2020) Network-level causal analysis of set-shifting during trail making test part B: a multimodal analysis of a glioma surgery case. Cortex 132:238–249. https://doi.org/10.1016/j.cortex.2020.08.021

    Article  PubMed  Google Scholar 

  22. Kinoshita M, Nakajima R, Shinohara H et al (2016) Chronic spatial working memory deficit associated with the superior longitudinal fasciculus: a study using voxel-based lesion-symptom mapping and intraoperative direct stimulation in right prefrontal glioma surgery. J Neurosurg 125(4):1024–1032. https://doi.org/10.3171/2015.10.JNS1591

    Article  PubMed  Google Scholar 

  23. Rossi M, Gay L, Conti Nibali M et al (2021) Challenging giant insular gliomas with brain mapping: evaluation of neurosurgical, neurological, neuropsychological, and quality of life results in a large mono-institutional series. Front Oncol 11. https://doi.org/10.3389/fonc.2021.629166

  24. Plaza M, du Boullay V, Perrault A, Chaby L, Capelle L (2014) A case of bilateral frontal tumors without “frontal syndrome.” Neurocase 20(6):671–683. https://doi.org/10.1080/13554794.2013.826696

    Article  CAS  PubMed  Google Scholar 

  25. Skrap M, Marin D, Ius T, Fabbro F, Tomasino B (2016) Brain mapping: a novel intraoperative neuropsychological approach. J Neurosurg 125(4):877–887. https://doi.org/10.3171/2015.10.JNS15740

    Article  PubMed  Google Scholar 

  26. Erez Y, Assem M, Coelho P et al (2021) Intraoperative mapping of executive function using electrocorticography for patients with low-grade gliomas. Acta Neurochir (Wien) 163(5):1299–1309. https://doi.org/10.1007/s00701-020-04646-6

    Article  PubMed  Google Scholar 

  27. Wager M, Du Boisgueheneuc F, Pluchon C et al (2013) Intraoperative monitoring of an aspect of executive functions: administration of the stroop test in 9 adult patients during awake surgery for resection of frontal glioma. Neurosurgery 72:ons169-ons180. https://doi.org/10.1227/NEU.0b013e31827bf1d6

  28. Puglisi G, Howells H, Sciortino T et al (2019) Frontal pathways in cognitive control: direct evidence from intraoperative stimulation and diffusion tractography. Brain 142(8):2451–2465. https://doi.org/10.1093/brain/awz178

    Article  PubMed  PubMed Central  Google Scholar 

  29. Puglisi G, Sciortino T, Rossi M et al (2018) Preserving executive functions in nondominant frontal lobe glioma surgery: an intraoperative tool. J Neurosurg 131(2):474–480. https://doi.org/10.3171/2018.4.JNS18393

    Article  PubMed  Google Scholar 

  30. Tomasino B, Guarracino I, Ius T, Skrap M (2023) Continuous real-time neuropsychological testing during resection phase in left and right prefrontal brain tumors. Curr Oncol 30(2):2007–2020. https://doi.org/10.3390/curroncol30020156

    Article  PubMed  PubMed Central  Google Scholar 

  31. Karbach J, Kray J (2016) Executive Functions. In: Strobach T, Karbach J, eds. Cognitive training: an overview of features and applications. Springer International Publishing 93–103. https://doi.org/10.1007/978-3-319-42662-4_9

  32. Niendam TA, Laird AR, Ray KL, Dean YM, Glahn DC, Carter CS (2012) Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 12(2):241–268. https://doi.org/10.3758/s13415-011-0083-5

    Article  PubMed  PubMed Central  Google Scholar 

  33. Corradi-Dell’Acqua C, Ueno K, Ogawa A, Cheng K, Rumiati RI, Iriki A (2008) Effects of shifting perspective of the self: an fMRI study. NeuroImage 40(4):1902–1911. https://doi.org/10.1016/j.neuroimage.2007.12.062

    Article  PubMed  Google Scholar 

  34. Baldo JV, Dronkers NF (2006) The role of inferior parietal and inferior frontal cortex in working memory. Neuropsychology 20:529–538. https://doi.org/10.1037/0894-4105.20.5.529

    Article  PubMed  Google Scholar 

  35. Mackey WE, Curtis CE (2017) Distinct contributions by frontal and parietal cortices support working memory. Sci Rep 7(1):6188. https://doi.org/10.1038/s41598-017-06293-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Curtis CE (2006) Prefrontal and parietal contributions to spatial working memory. Neuroscience 139(1):173–180. https://doi.org/10.1016/j.neuroscience.2005.04.070

    Article  CAS  PubMed  Google Scholar 

  37. Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J (2007) Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci 27(29):7807–7816. https://doi.org/10.1523/JNEUROSCI.0962-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Olson IR, Page K, Moore KS, Chatterjee A, Verfaellie M (2006) Working memory for conjunctions relies on the medial temporal lobe. J Neurosci 26(17):4596–4601. https://doi.org/10.1523/JNEUROSCI.1923-05.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Jeneson A, Squire LR (2012) Working memory, long-term memory, and medial temporal lobe function. Learn Mem 19(1):15–25. https://doi.org/10.1101/lm.024018.111

    Article  PubMed  PubMed Central  Google Scholar 

  40. Friedman NP, Robbins TW (2022) The role of prefrontal cortex in cognitive control and executive function. Neuropsychopharmacology 47(1):72–89. https://doi.org/10.1038/s41386-021-01132-0

    Article  PubMed  Google Scholar 

  41. Kovac S, Kahane P, Diehl B (2016) Seizures induced by direct electrical cortical stimulation – mechanisms and clinical considerations. Clin Neurophysiol 127(1):31–39. https://doi.org/10.1016/j.clinph.2014.12.009

    Article  PubMed  Google Scholar 

  42. Morshed RA, Young JS, Lee AT, Berger MS, Hervey-Jumper SL (2020) Clinical pearls and methods for intraoperative awake language mapping. Neurosurgery 89(2):143–153. https://doi.org/10.1093/neuros/nyaa440

    Article  PubMed Central  Google Scholar 

  43. Hariz MI (2002) Complications of deep brain stimulation surgery. Mov Disord 17(S3):S162–S166. https://doi.org/10.1002/mds.10159

    Article  PubMed  Google Scholar 

Download references

Funding

This research received no external funding.

Author information

Authors and Affiliations

  1. Section of Neurosurgery, Department of Surgery, Aga Khan University Hospital, Karachi, Pakistan

    Rabeet Tariq, Hafiza Fatima Aziz, Shahier Paracha, Noman Ahmed, Saqib Kamran Bakhshi & Syed Ather Enam

  2. Department of Neurosurgery, Southmead Hospital, NHS North Bristol Trust, Bristol, UK

    Muhammad Waqas Saeed Baqai

  3. College of Medicine, University of Kentucky, Lexington, USA

    Annabel McAtee

  4. Department of Neurology, University of Kentucky College of Medicine, Kentucky Neuroscience Institute, Lexington, KY, USA

    Timothy J. Ainger

  5. Department of Neurosurgery, Kentucky Neuroscience Institute (KNI), University of Kentucky, Lexington, USA

    Farhan A. Mirza

Authors
  1. Rabeet Tariq
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hafiza Fatima Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shahier Paracha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noman Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Waqas Saeed Baqai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Saqib Kamran Bakhshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Annabel McAtee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Timothy J. Ainger
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Farhan A. Mirza
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Syed Ather Enam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Syed Ather Enam.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

No humans and/or animals were involved.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tariq, R., Aziz, H.F., Paracha, S. et al. Intraoperative mapping and preservation of executive functions in awake craniotomy: a systematic review. Neurol Sci (2024). https://doi.org/10.1007/s10072-024-07475-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10072-024-07475-y

Keywords

Search

Navigation