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

Restricted access

OBJECTIVE

Although the right prefrontal region is regarded as a silent area, chronic deficits of the executive function, including working memory (WM), could occur after resection of a right prefrontal glioma. This may be overlooked by postoperative standard examinations, and the disabilities could affect the patient's professional life. The right prefrontal region is a part of the frontoparietal network and is subserved by the superior longitudinal fasciculus (SLF); however, the role of the SLF in spatial WM is unclear. This study investigated a persistent spatial WM deficit in patients who underwent right prefrontal glioma resection, and evaluated the relationship between the spatial WM deficit and the SLF.

METHODS

Spatial WM was examined in 24 patients who underwent prefrontal glioma resection (right, n = 14; left, n = 10) and in 14 healthy volunteers using a spatial 2-back task during the long-term postoperative period. The neural correlates of spatial WM were evaluated using lesion mapping and voxel-based lesion-symptom mapping. In addition, the spatial 2-back task was performed during surgery under direct subcortical electrical stimulation in 2 patients with right prefrontal gliomas.

RESULTS

Patients with a right prefrontal lesion had a significant chronic spatial WM deficit. Voxel-based lesion-symptom mapping analysis revealed a significant correlation between spatial WM deficit and the region that overlapped the first and second segments of the SLF (SLF I and SLF II). Two patients underwent awake surgery and had difficulties providing the correct responses in the spatial 2-back task with direct subcortical electrical stimulation on the SLF I, which was preserved and confirmed by postoperative diffusion tensor imaging tractography. These patients exhibited no spatial WM deficits during the postoperative immediate and long-term periods.

CONCLUSIONS

Spatial WM deficits may persist in patients who undergo resection of the tumor located in the right prefrontal brain parenchyma. Injury to the dorsal frontoparietal subcortical white matter pathway, i.e., the SLF I or SLF I and II, could play a causal role in this chronic deficit. A persistent spatial WM deficit, without motor and language deficits, could affect the professional life of the patient. In such cases, awake surgery would be useful to detect the spatial WM network with appropriate task during tumor exploration.

ABBREVIATIONSDES = direct electrical stimulation; DTI = diffusion tensor imaging; DW = diffusion weighted; FDR = false discovery rate; MNI = Montreal Neurological Institute; SLF = superior longitudinal fasciculus; VLSM = voxel-based lesion-symptom mapping; VOI = volume of interest; WM = working memory.
Article Information

Contributor Notes

INCLUDE WHEN CITING Published online February 19, 2016; DOI: 10.3171/2015.10.JNS1591.

Dr. Kinoshita and Ms. Nakajima contributed equally to this work.

Correspondence Yutaka Hayashi, Department of Neurosurgery, Kanazawa University, 13-1 Takaramachi, Kanazawa 920-8641, Japan. email: yuh@med.kanazawa-u.ac.jp.

© AANS, except where prohibited by US copyright law.

Headings
References
  • 1

    Aaronson NKTaphoorn MJBHeimans JJPostma TJGundy CMBeute GN: Compromised health-related quality of life in patients with low-grade glioma. J Clin Oncol 29:443044352011

    • Search Google Scholar
    • Export Citation
  • 2

    Baddeley A: Working memory: looking back and looking forward. Nat Rev Neurosci 4:8298392003

  • 3

    Bartolomeo PThiebaut de Schotten MChica AB: Brain networks of visuospatial attention and their disruption in visual neglect. Front Hum Neurosci 6:1102012

    • Search Google Scholar
    • Export Citation
  • 4

    Bartolomeo PThiebaut de Schotten MDoricchi F: Left unilateral neglect as a disconnection syndrome. Cereb Cortex 17:247924902007

    • Search Google Scholar
    • Export Citation
  • 5

    Bates EWilson SMSaygin APDick FSereno MIKnight RT: Voxel-based lesion-symptom mapping. Nat Neurosci 6:4484502003

  • 6

    Brett MLeff APRorden CAshburner J: Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 14:4865002001

    • Search Google Scholar
    • Export Citation
  • 7

    Catani MThiebaut de Schotten M: Atlas of Human Brain Connections New YorkOxford University Press2012

  • 8

    Corbetta MKincade MJLewis CSnyder AZSapir A: Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci 8:160316102005

    • Search Google Scholar
    • Export Citation
  • 9

    Corbetta MShulman GL: Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:2012152002

  • 10

    Courtney SMPetit LMaisog JMUngerleider LGHaxby JV: An area specialized for spatial working memory in human frontal cortex. Science 279:134713511998

    • Search Google Scholar
    • Export Citation
  • 11

    Curtis CE: Prefrontal and parietal contributions to spatial working memory. Neuroscience 139:1731802006

  • 12

    du Boisgueheneuc FLevy RVolle ESeassau MDuffau HKinkingnehun S: Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:331533282006

    • Search Google Scholar
    • Export Citation
  • 13

    Duffau HPeggy Gatignol STMandonnet ECapelle LTaillandier L: Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 109:4614712008

    • Search Google Scholar
    • Export Citation
  • 14

    Gazzaley ANobre AC: Top-down modulation: bridging selective attention and working memory. Trends Cogn Sci 16:1291352012

  • 15

    Heilman KWatson RValenstein ENeglect and related disorders. Heilman KValenstein E: Clinical Neuropsychology ed 3New YorkOxford University Press1993. 279336

    • Search Google Scholar
    • Export Citation
  • 16

    Hofmann WSchmeichel BJBaddeley AD: Executive functions and self-regulation. Trends Cogn Sci 16:1741802012

  • 17

    Ius TAngelini EThiebaut de Schotten MMandonnet EDuffau 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 56:99210002011

    • Search Google Scholar
    • Export Citation
  • 18

    Kamali AFlanders AEBrody JHunter JVHasan KM: Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219:2692812014

    • Search Google Scholar
    • Export Citation
  • 19

    Klein MDuffau HDe Witt Hamer PC: Cognition and resective surgery for diffuse infiltrative glioma: an overview. J Neurooncol 108:3093182012

    • Search Google Scholar
    • Export Citation
  • 20

    Klingberg T: Development of a superior frontal-intraparietal network for visuo-spatial working memory. Neuropsychologia 44:217121772006

    • Search Google Scholar
    • Export Citation
  • 21

    Kravitz DJSaleem KSBaker CIMishkin M: A new neural framework for visuospatial processing. Nat Rev Neurosci 12:2172302011

  • 22

    Levy RGoldman-Rakic PS: Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23322000

    • Search Google Scholar
    • Export Citation
  • 23

    Makris NKennedy DNMcInerney SSorensen AGWang RCaviness VS Jr: Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15:8548692005

    • Search Google Scholar
    • Export Citation
  • 24

    Malhotra PJäger HRParton AGreenwood RPlayford EDBrown MM: Spatial working memory capacity in unilateral neglect. Brain 128:4244352005

    • Search Google Scholar
    • Export Citation
  • 25

    Martino JDe Witt Hamer PCBerger MSLawton MTArnold CMde Lucas EM: Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct 218:1051212013

    • Search Google Scholar
    • Export Citation
  • 26

    Mayer JSBittner RANikolić DBledowski CGoebel RLinden DE: Common neural substrates for visual working memory and attention. Neuroimage 36:4414532007

    • Search Google Scholar
    • Export Citation
  • 27

    Mesulam MM: Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci 354:132513461999

    • Search Google Scholar
    • Export Citation
  • 28

    Müller NGKnight RT: The functional neuroanatomy of working memory: contributions of human brain lesion studies. Neuroscience 139:51582006

    • Search Google Scholar
    • Export Citation
  • 29

    Rorden CKarnath HO: Using human brain lesions to infer function: a relic from a past era in the fMRI age?. Nat Rev Neurosci 5:8138192004

    • Search Google Scholar
    • Export Citation
  • 30

    Rorden CKarnath HOBonilha L: Improving lesion-symptom mapping. J Cogn Neurosci 19:108110882007

  • 31

    Salazar RFDotson NMBressler SLGray CM: Content-specific frontoparietal synchronization during visual working memory. Science 338:109711002012

    • Search Google Scholar
    • Export Citation
  • 32

    Schmahmann JDPandya DN: Fiber Pathways of the Brain New YorkOxford University Press2006

  • 33

    Smith EEJonides JKoeppe RA: Dissociating verbal and spatial working memory using PET. Cereb Cortex 6:11201996

  • 34

    Szelényi ABello LDuffau HFava EFeigl GCGalanda M: Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 28:2E72010

    • Search Google Scholar
    • Export Citation
  • 35

    Thiebaut de Schotten MDell'Acqua FForkel SJSimmons AVergani FMurphy DG: A lateralized brain network for visuospatial attention. Nat Neurosci 14:124512462011

    • Search Google Scholar
    • Export Citation
  • 36

    Thiebaut de Schotten MDell'Acqua FValabregue RCatani M: Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48:82962012

    • Search Google Scholar
    • Export Citation
  • 37

    Thiebaut de Schotten MTomaiuolo FAiello MMerola SSilvetti MLecce F: Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete virtual “in vivo” tractography dissection. Cereb Cortex 24:6917062014

    • Search Google Scholar
    • Export Citation
  • 38

    Thiebaut de Schotten MUrbanski MDuffau HVolle ELévy RDubois B: Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309:222622282005

    • Search Google Scholar
    • Export Citation
  • 39

    Ungerleider LGCourtney SMHaxby JV: A neural system for human visual working memory. Proc Natl Acad Sci U S A 95:8838901998

  • 40

    Vallar GBello LBricolo ECastellano ACasarotti AFalini A: Cerebral correlates of visuospatial neglect: a direct cerebral stimulation study. Hum Brain Mapp 35:133413502014

    • Search Google Scholar
    • Export Citation
  • 41

    van Asselen MKessels RPNeggers SFKappelle LJFrijns CJPostma A: Brain areas involved in spatial working memory. Neuropsychologia 44:118511942006

    • Search Google Scholar
    • Export Citation
  • 42

    Verdon VSchwartz SLovblad KOHauert CAVuilleumier P: Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain 133:8808942010

    • Search Google Scholar
    • Export Citation
  • 43

    Vestergaard MMadsen KSBaaré WFSkimminge AEjersbo LRRamsøy TZ: White matter microstructure in superior longitudinal fasciculus associated with spatial working memory performance in children. J Cogn Neurosci 23:213521462011

    • Search Google Scholar
    • Export Citation
  • 44

    Walter HBretschneider VGrön GZurowski BWunderlich APTomczak R: Evidence for quantitative domain dominance for verbal and spatial working memory in frontal and parietal cortex. Cortex 39:8979112003

    • Search Google Scholar
    • Export Citation
TrendMD
Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 495 426 95
PDF Downloads 231 180 11
EPUB Downloads 0 0 0
PubMed
Google Scholar