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Does Stroke Imaging Provide Insights into the Neural Basis of Cognition?

  • Paresh A. Malhotra
  • Charlotte Russell
Neuroimaging (DJ Brooks, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Neuroimaging

Abstract

Since the advent of in vivo imaging, first with CT, and then MRI, structural neuroimaging in patients has been widely used as a tool to explore the neural correlates of a wide variety of cognitive functions. Findings from studies using this methodology have formed a core component of current accounts of cognition, but there are a number of problematic issues related to inferring cognitive functions from structural imaging data in stroke and more generally, lesion-based neuropsychology as a whole. This review addresses these concerns in the context of spatial neglect, a common disorder most frequently encountered following right hemisphere stroke. Recent literature, including attempts to address some of these questions, is discussed. Novel approaches and findings from related fields that may help to put stroke-based lesion mapping studies into perspective are reviewed, allowing critical but constructive evaluation of previous work in the field.

Keywords

Stroke Neuropsychology Lesion mapping Neglect Attention 

Notes

Acknowledgments

Dr Malhotra is funded by a HEFCE Clinical Senior Lectureship and receives support from the National Institute for Health Research (NIHR) Imperial Biomedical Research Centre at Imperial College.

Compliance with Ethics Guidelines

Conflict of Interest

Paresh A. Malhotra and Charlotte Russell declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Broca P. Perte de la parole, ramollissement chronique et destruction partielle du lobe antérieur gauche du cerveau. Bull Soc Anthropologique. 1861;2:235–8.Google Scholar
  2. 2.
    Davis CL, Oishi K, Faria AV, et al. White matter tracts critical for recognition of sarcasm. Neurocase 2015:1–8 doi:  10.1080/13554794.2015.1024137.
  3. 3.
    Leff AP, Schofield TM, Crinion JT, et al. The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: evidence from 210 patients with stroke. Brain. 2009;132(Pt 12):3401–10. doi: 10.1093/brain/awp273.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Karnath HO, Fruhmann Berger M, Kuker W, et al. The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex. 2004;14(10):1164–72. doi: 10.1093/cercor/bhh076.PubMedCrossRefGoogle Scholar
  5. 5.
    Doricchi F, Tomaiuolo F. The anatomy of neglect without hemianopia: a key role for parietal-frontal disconnection? Neuroreport. 2003;14(17):2239–43. doi: 10.1097/01.wnr.0000091132.75061.64.PubMedCrossRefGoogle Scholar
  6. 6.
    Hillis AE, Newhart M, Heidler J, et al. Anatomy of spatial attention: insights from perfusion imaging and hemispatial neglect in acute stroke. J Neurosci. 2005;25(12):3161–7.PubMedCrossRefGoogle Scholar
  7. 7.
    Mort DJ, Malhotra P, Mannan SK, et al. The anatomy of visual neglect. Brain. 2003;126(Pt 9):1986–97.PubMedCrossRefGoogle Scholar
  8. 8.
    Ringman JM, Saver JL, Woolson RF, et al. Frequency, risk factors, anatomy, and course of unilateral neglect in an acute stroke cohort. Neurology. 2004;63(3):468–74.PubMedCrossRefGoogle Scholar
  9. 9.
    Verdon V, Schwartz S, Lovblad KO, et al. Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain. 2010;133(Pt 3):880–94. doi: 10.1093/brain/awp305.PubMedCrossRefGoogle Scholar
  10. 10.
    Doricchi F, Thiebaut de Schotten M, Tomaiuolo F, et al. White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness. Cortex. 2008;44(8):983–95. doi: 10.1016/j.cortex.2008.03.006.PubMedCrossRefGoogle Scholar
  11. 11.•
    Lunven M, Thiebaut De Schotten M, Bourlon C, et al. White matter lesional predictors of chronic visual neglect: a longitudinal study. Brain : J Neurol 2015 doi:  10.1093/brain/awu389. This paper adds to the body of work emphasizing the importance of disconnection and network dysfunction in neglect.
  12. 12.
    Urbanski M, Thiebaut de Schotten M, Rodrigo S, et al. Brain networks of spatial awareness: evidence from diffusion tensor imaging tractography. J Neurol Neurosurg Psychiatry. 2008;79(5):598–601.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Naeser MA, Hayward RW. Lesion localization in aphasia with cranial computed tomography and the Boston Diagnostic Aphasia Exam. Neurology. 1978;28(6):545–51.PubMedCrossRefGoogle Scholar
  14. 14.
    Vallar G, Perani D. The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man. Neuropsychologia. 1986;24(5):609–22.PubMedCrossRefGoogle Scholar
  15. 15.
    DeWitt LD, Grek AJ, Buonanno FS, et al. MRI and the study of aphasia. Neurology. 1985;35(6):861–5.PubMedCrossRefGoogle Scholar
  16. 16.
    Karnath HO, Ferber S, Himmelbach M. Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature. 2001;411(6840):950–3. doi: 10.1038/35082075.PubMedCrossRefGoogle Scholar
  17. 17.
    Rorden C, Karnath HO. Using human brain lesions to infer function: a relic from a past era in the fMRI age? Nat Rev Neurosci. 2004;5(10):813–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Bates E, Wilson SM, Saygin AP, et al. Voxel-based lesion-symptom mapping. Nat Neurosci. 2003;6(5):448–50.PubMedGoogle Scholar
  19. 19.
    Catani M. Diffusion tensor magnetic resonance imaging tractography in cognitive disorders. Curr Opin Neurol. 2006;19(6):599–606. doi: 10.1097/01.wco.0000247610.44106.3f.PubMedCrossRefGoogle Scholar
  20. 20.
    Thiebaut de Schotten M, Tomaiuolo F, Aiello M, et al. 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. 2014;24(3):691–706. doi: 10.1093/cercor/bhs351.PubMedCrossRefGoogle Scholar
  21. 21.
    Forkel SJ, Thiebaut de Schotten M, Dell’Acqua F, et al. Anatomical predictors of aphasia recovery: a tractography study of bilateral perisylvian language networks. Brain. 2014;137(Pt 7):2027–39. doi: 10.1093/brain/awu113.PubMedCrossRefGoogle Scholar
  22. 22.•
    Mah YH, Husain M, Rees G, et al. Human brain lesion-deficit inference remapped. Brain: J Neurol. 2014;137(Pt 9):2522–31. doi: 10.1093/brain/awu164. Mah et al. used high dimensional analysis to examine lesion data from over 581 patients, and suggested that the majority of stroke lesion mapping studies to-date are subject to an inherent anatomical bias. This confound is a potential issue for all studies that only include lesions secondary to ischaemic stroke. CrossRefGoogle Scholar
  23. 23.
    Bolognini N, Ro T. Transcranial magnetic stimulation: disrupting neural activity to alter and assess brain function. J Neurosci. 2010;30(29):9647–50. doi: 10.1523/JNEUROSCI.1990-10.2010.PubMedCrossRefGoogle Scholar
  24. 24.
    Thiebaut de Schotten M, Urbanski M, Duffau H, et al. Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science. 2005;309(5744):2226–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Heilman KM, Watson RT, Valenstein E. Neglect and related disorders. In: Heilman KM, Valenstein E, editors. Clinical neuropsychology. 4th ed. New York: OUP; 2003. p. 296–346.Google Scholar
  26. 26.
    Churchland PS. Brain-wise: studies in neurophilosophy. Cambridge: MIT Press; 2002.Google Scholar
  27. 27.
    Genova L. Left neglected : a novel. 1st Gallery Books hardcover ed. New York: Gallery Books; 2011.Google Scholar
  28. 28.
    Corbetta M, Shulman GL. Spatial neglect and attention networks. Annu Rev Neurosci. 2011;34:569–99. doi: 10.1146/annurev-neuro-061010-113731.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Heilman KM, Van Den Abell T. Right hemisphere dominance for attention: the mechanism underlying hemispheric asymmetries of inattention (neglect). Neurology. 1980;30(3):327–30.PubMedCrossRefGoogle Scholar
  30. 30.
    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 Ser B Biol Sci. 1999;354(1387):1325–46. doi: 10.1098/rstb.1999.0482.CrossRefGoogle Scholar
  31. 31.•
    Vuilleumier P. Mapping the functional neuroanatomy of spatial neglect and human parietal lobe functions: progress and challenges. Ann N Y Acad Sci. 2013;1296:50–74. doi: 10.1111/nyas.12161. A clear-sighted review of the field, with an acute appreciation of the problems that beset attempts to map a clinical syndrome to a single brain region. PubMedCrossRefGoogle Scholar
  32. 32.
    Karnath HO, Rorden C. The anatomy of spatial neglect. Neuropsychologia. 2012;50(6):1010–7. doi: 10.1016/j.neuropsychologia.2011.06.027.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Stone SP, Wilson B, Wroot A, et al. The assessment of visuo-spatial neglect after acute stroke. J Neurol Neurosurg Psychiatry. 1991;54(4):345–50.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Azouvi P, Samuel C, Louis-Dreyfus A, et al. Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. J Neurol Neurosurg Psychiatry. 2002;73(2):160–6.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Gauthier L, Deahault F, Joanette Y. The bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol. 1989;11:49–54.Google Scholar
  36. 36.
    Jehkonen M, Laihosalo M, Koivisto AM, et al. Fluctuation in spontaneous recovery of left visual neglect: a 1-year follow-up. Eur Neurol. 2007;58(4):210–4.PubMedCrossRefGoogle Scholar
  37. 37.
    Bailey MJ, Riddoch MJ, Crome P. Treatment of visual neglect in elderly patients with stroke: a single-subject series using either a scanning and cueing strategy or a left-limb activation strategy. Phys Ther. 2002;82(8):782–97.PubMedGoogle Scholar
  38. 38.
    Husain M, Rorden C. Non-spatially lateralized mechanisms in hemispatial neglect. Nature reviews. Neuroscience. 2003;4(1):26–36. doi: 10.1038/nrn1005.PubMedGoogle Scholar
  39. 39.•
    Malhotra PA, Soto D, Li K, et al. Reward modulates spatial neglect. J Neurol Neurosurg Psychiatry. 2013;84(4):366–9. doi: 10.1136/jnnp-2012-303169. The first empirical demonstration of the effect of anticipated reward on impaired attention in stroke patients. This result suggests that motivational function may have an important role to play in attentional performance following stroke. PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Mesulam MM. Principles of behavioral neurology. Philadelphia: F.A. Davis; 1985.Google Scholar
  41. 41.
    Na DL, Adair JC, Williamson DJ, et al. Dissociation of sensory-attentional from motor-intentional neglect. J Neurol Neurosurg Psychiatry. 1998;64(3):331–8.PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Bisiach E, Geminiani G, Berti A, et al. Perceptual and premotor factors of unilateral neglect. Neurology. 1990;40(8):1278–81.PubMedCrossRefGoogle Scholar
  43. 43.
    Malhotra P, Jager HR, Parton A, et al. Spatial working memory capacity in unilateral neglect. Brain. 2005;128(Pt 2):424–35. doi: 10.1093/brain/awh372.PubMedGoogle Scholar
  44. 44.
    Husain M, Kennard C. Visual neglect associated with frontal lobe infarction. J Neurol. 1996;243(9):652–7.PubMedCrossRefGoogle Scholar
  45. 45.
    Watson RT, Valenstein E, Heilman KM. Thalamic neglect. Possible role of the medial thalamus and nucleus reticularis in behavior. Arch Neurol. 1981;38(8):501–6.PubMedCrossRefGoogle Scholar
  46. 46.
    Leibovitch FS, Black SE, Caldwell CB, et al. Brain-behavior correlations in hemispatial neglect using CT and SPECT: the Sunnybrook Stroke Study. Neurology. 1998;50(4):901–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Karnath HO, Rennig J, Johannsen L, et al. The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain. 2011;134(Pt 3):903–12. doi: 10.1093/brain/awq355.PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Smith DV, Clithero JA, Rorden C, et al. Decoding the anatomical network of spatial attention. Proc Natl Acad Sci U S A. 2013;110(4):1518–23. doi: 10.1073/pnas.1210126110.PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Corbetta M, Kincade MJ, Lewis C, et al. Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci. 2005;8(11):1603–10. doi: 10.1038/nn1574.PubMedCrossRefGoogle Scholar
  50. 50.
    Binder J, Marshall R, Lazar R, et al. Distinct syndromes of hemineglect. Arch Neurol. 1992;49(11):1187–94.PubMedCrossRefGoogle Scholar
  51. 51.
    Rorden C, Fruhmann Berger M, Karnath HO. Disturbed line bisection is associated with posterior brain lesions. Brain Res. 2006;1080(1):17–25. doi: 10.1016/j.brainres.2004.10.071.PubMedCrossRefGoogle Scholar
  52. 52.
    Committeri G, Pitzalis S, Galati G, et al. Neural bases of personal and extrapersonal neglect in humans. Brain : J Neurol. 2007;130(Pt 2):431–41. doi: 10.1093/brain/awl265.CrossRefGoogle Scholar
  53. 53.
    Chechlacz M, Rotshtein P, Humphreys GW. Neuroanatomical dissections of unilateral visual neglect symptoms: ALE meta-analysis of lesion-symptom mapping. Front Hum Neurosci. 2012;6:230. doi: 10.3389/fnhum.2012.00230.PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Molenberghs P, Sale MV, Mattingley JB. Is there a critical lesion site for unilateral spatial neglect? A meta-analysis using activation likelihood estimation. Front Hum Neurosci. 2012;6:78. doi: 10.3389/fnhum.2012.00078.PubMedCentralPubMedCrossRefGoogle Scholar
  55. 55.
    Stone SP, Halligan PW, Greenwood RJ. The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. Age Ageing. 1993;22(1):46–52.PubMedCrossRefGoogle Scholar
  56. 56.•
    Bonato M. Neglect and extinction depend greatly on task demands: a review. Front Hum Neurosci. 2012;6:195. doi: 10.3389/fnhum.2012.00195. An important paper stressing the point that neglect and related deficits may go undiagnosed unless sophisticated targeted behavioural testing is carried out. PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Becker H, Desch H, Hacker H, et al. CT fogging effect with ischemic cerebral infarcts. Neuroradiology. 1979;18(4):185–92.PubMedCrossRefGoogle Scholar
  58. 58.
    Ricci PE, Burdette JH, Elster AD, et al. A comparison of fast spin-echo, fluid-attenuated inversion-recovery, and diffusion-weighted MR imaging in the first 10 days after cerebral infarction. AJNR Am J Neuroradiol. 1999;20(8):1535–42.PubMedGoogle Scholar
  59. 59.
    Hillis AE, Wityk RJ, Barker PB, et al. Subcortical aphasia and neglect in acute stroke: the role of cortical hypoperfusion. Brain. 2002;125(Pt 5):1094–104.PubMedCrossRefGoogle Scholar
  60. 60.
    Samuelsson H, Jensen C, Ekholm S, et al. Anatomical and neurological correlates of acute and chronic visuospatial neglect following right hemisphere stroke. Cortex. 1997;33(2):271–85.PubMedCrossRefGoogle Scholar
  61. 61.
    Shinoura N, Suzuki Y, Yamada R, et al. Damage to the right superior longitudinal fasciculus in the inferior parietal lobe plays a role in spatial neglect. Neuropsychologia. 2009;47(12):2600–3. doi: 10.1016/j.neuropsychologia.2009.05.010.PubMedCrossRefGoogle Scholar
  62. 62.••
    Umarova RM, Reisert M, Beier TU, et al. Attention-network specific alterations of structural connectivity in the undamaged white matter in acute neglect. Hum Brain Mapp. 2014;35(9):4678–92. doi: 10.1002/hbm.22503. A very interesting study showing contralesional white matter changes in patients with neglect. Further work is necessary to pin down how exactly this relates to dysfunction and recovery. PubMedCrossRefGoogle Scholar
  63. 63.
    He BJ, Snyder AZ, Vincent JL, et al. Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron. 2007;53(6):905–18. doi: 10.1016/j.neuron.2007.02.013.PubMedCrossRefGoogle Scholar
  64. 64.
    Umarova RM, Saur D, Kaller CP, et al. Acute visual neglect and extinction: distinct functional state of the visuospatial attention system. Brain : J Neurol. 2011;134(Pt 11):3310–25. doi: 10.1093/brain/awr220.CrossRefGoogle Scholar
  65. 65.
    Mesulam MM. A cortical network for directed attention and unilateral neglect. Ann Neurol. 1981;10(4):309–25. doi: 10.1002/ana.410100402.PubMedCrossRefGoogle Scholar
  66. 66.
    Sparing R, Thimm M, Hesse MD, et al. Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. Brain : J Neurol. 2009;132(Pt 11):3011–20. doi: 10.1093/brain/awp154.CrossRefGoogle Scholar
  67. 67.••
    Corbetta M, Ramsey L, Callejas A, et al. Common behavioral clusters and subcortical anatomy in stroke. Neuron. 2015;85(5):927–41. doi: 10.1016/j.neuron.2015.02.027. An anatomical study looking at a large sample of relatively unselected stroke patients, allowing the investigators to carefully examine anatomy and multiple behavioural deficits in tandem. The results highlight the importance of white matter damage and network dysfunction, and also begin to dissect the behavioural factors that contribute to impaired performance in separate cognitive domains. PubMedCrossRefGoogle Scholar
  68. 68.
    Nachev P. The first step in modern lesion-deficit analysis. Brain : J Neurol. 2014. doi: 10.1093/brain/awu275.Google Scholar
  69. 69.
    Levine DN, Warach JD, Benowitz L, et al. Left spatial neglect: effects of lesion size and premorbid brain atrophy on severity and recovery following right cerebral infarction. Neurology. 1986;36(3):362–6.PubMedCrossRefGoogle Scholar
  70. 70.
    Bahrainwala ZS, Hillis AE, Dearborn J, et al. Neglect performance in acute stroke is related to severity of white matter hyperintensities. Cerebrovasc Dis. 2014;37(3):223–30. doi: 10.1159/000357661.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Bellgrove MA, Chambers CD, Johnson KA, et al. Dopaminergic genotype biases spatial attention in healthy children. Mol Psychiatry. 2007;12(8):786–92. doi: 10.1038/sj.mp.4002022.PubMedCrossRefGoogle Scholar
  72. 72.
    Bartolomeo P. The quest for the ‘critical lesion site’ in cognitive deficits: problems and perspectives. Cortex J Devoted Study Nerv Syst Behav. 2011;47(8):1010–2. doi: 10.1016/j.cortex.2010.11.007.CrossRefGoogle Scholar
  73. 73.
    Shallice T, Skrap M. Localisation through operation for brain tumour: a reply to Karnath and Steinbach. Cortex J Devoted Study Nerv Syst Behav. 2011;47(8):1007–9. doi: 10.1016/j.cortex.2010.12.006.CrossRefGoogle Scholar
  74. 74.
    Zilli EM, Heilman KM. Allocentric spatial neglect with posterior cortical atrophy. Neurocase. 2015;21(2):190–7. doi: 10.1080/13554794.2013.878731.PubMedCrossRefGoogle Scholar
  75. 75.
    Andrade K, Samri D, Sarazin M, et al. Visual neglect in posterior cortical atrophy. BMC Neurol. 2010;10:68. doi: 10.1186/1471-2377-10-68.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.•
    Cipolotti L, Healy C, Chan E, et al. The impact of different aetiologies on the cognitive performance of frontal patients. Neuropsychologia. 2015;68:21–30. doi: 10.1016/j.neuropsychologia.2014.12.025. An important study examining whether different pathological aetiologies led to variation in cognitive profiles in frontal patients. The lack of difference between patient subgroups suggests that grouping patients together may not be as problematic as was previously thought. PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Centre for Restorative Neuroscience, Division of Brain SciencesImperial College LondonLondonUK
  2. 2.Department of Psychology, Institute of Psychiatry, Psychology and NeuroscienceKing’s College LondonLondonUK

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