Advertisement

Experimental Brain Research

, Volume 232, Issue 6, pp 1971–1987 | Cite as

Statistical and perceptual updating: correlated impairments in right brain injury

  • Elisabeth Stöttinger
  • Alex Filipowicz
  • Elahe Marandi
  • Nadine Quehl
  • James Danckert
  • Britt Anderson
Research Article

Abstract

It has been hypothesized that many of the cognitive impairments commonly seen after right brain damage (RBD) can be characterized as a failure to build or update mental models. We (Danckert et al. in Neglect as a disorder of representational updating. NOVA Open Access, New York, 2012a; Cereb Cortex 22:2745–2760, 2012b) were the first to directly assess the association between RBD and updating and found that RBD patients were unable to exploit a strongly biased play strategy in their opponent in the children’s game rock, paper, scissors. Given that this game required many other cognitive capacities (i.e., working memory, sustained attention, reward processing), RBD patients could have failed this task for various reasons other than a failure to update. To assess the generality of updating deficits after RBD, we had RBD, left brain-damaged (LBD) patients and healthy controls (HCs) describe line drawings that evolved gradually from one figure (e.g., rabbit) to another (e.g., duck) in addition to the RPS updating task. RBD patients took significantly longer to alter their perceptual report from the initial object to the final object than did LBD patients and HCs. Although both patient groups performed poorly on the RPS task, only the RBD patients showed a significant correlation between the two, very different, updating tasks. We suggest these data indicate a general deficiency in the ability to update mental representations following RBD.

Keywords

Right brain damage Mental representations Updating failures Ambiguous figures 

Notes

Acknowledgments

Natural Sciences and Engineering Research Council (http://www.nserc-crsng.gc.ca/index_eng.asp) of Canada Discovery (#261628-07), Canada Research Chair grants, Heart and Stroke Foundation of Ontario (http://www.heartandstroke.on.ca; #NA 6999 to J.D.) and Canadian Institutes of Health Research (http://www.cihr-irsc.gc.ca/e/193.html; #219972 operating grant to J.D. and B.A.). The above-mentioned funding agencies had no role in the study design, data collection and analysis, decision to publish or the preparation of the manuscript. We thank Elizabeth Kurusi for her assistance with patient recruitment and data collection and Linda Carson for her help in improvement the quality of two of the picture sets. We thank Nazanin Mohammadi Sepahvand for her help with data analysis. Finally, we would like to thank all of our participants for their time and effort in this experiment.

References

  1. Appelros P, Karlsson GM, Seiger A, Nydevik I (2002) Neglect and anosognosia after first-ever stroke: incidence and relationship to disability. J Rehabil Med 34:215–220PubMedCrossRefGoogle Scholar
  2. Aslin RN, Newport EL (2012) Statistical learning from acquiring specific items to forming general rules. Curr Dir Psychol Sci 21:170–176. doi: 10.1177/0963721412436806 PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bartolomeo P, De Schotten MT, Chica AB (2012) Brain networks of visuospatial attention and their disruption in visual neglect. Front hum neurosci 6. doi: 10.3389/fnhum.2012.00110
  4. Basso G, Nichelli P, Frassinetti F, di Pellegrino G (1996) Time perception in a neglected space. Neuroreport 7:2111–2114PubMedCrossRefGoogle Scholar
  5. Bernstein LJ, Cooper LA (1997) Direction of motion influences perceptual identification of ambiguous figures. J Exp Psychol Hum Percept Perform 23:721–737. doi: 10.1037/0096-1523.23.3.721 PubMedCrossRefGoogle Scholar
  6. Bischoff-Grethe A, Hazeltine E, Bergren L, Ivry RB, Grafton ST (2009) The influence of feedback valence in associative learning. Neuroimage 44:243–251. doi: 10.1016/j.neuroimage.2008.08.038 PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bonato M (2012). Neglect and extinction depend greatly on task demands: a review. Front hum neurosci 6. doi:  10.3389/fnhum.2012.00195
  8. Bonneh YS, Pavlovskaya M, Ring H, Soroker N (2004) Abnormal binocular rivalry in unilateral neglect: evidence for a nonspatial mechanism of extinction. Neuroreport 15:473–477PubMedCrossRefGoogle Scholar
  9. Bowen A, Lincoln NB (2007) Rehabilitation for spatial neglect improves test performance but not disability. Stroke 38:2869–2870. doi: 10.1161/STROKEAHA.107.490227 CrossRefGoogle Scholar
  10. Bowen A, McKenna K, Tallis RC (1999) Reasons for variability in the reported rate of occurrence of unilateral spatial neglect after stroke. Stroke 30:1196–1202. doi: 10.1161/01.STR.30.6.1196 PubMedCrossRefGoogle Scholar
  11. Britz J, Landis T, Michel CM (2009) Right parietal brain activity precedes perceptual alternation of bistable stimuli. Cereb Cortex 19:55–65. doi: 10.1093/cercor/bhn056 PubMedCrossRefGoogle Scholar
  12. Brownell HH, Michel D, Powelson J, Gardner H (1983) Surprise but not coherence: sensitivity to verbal humor in right-hemisphere patients. Brain Lang 18:20–27. doi: 10.1016/0093-934X(83)90002-0 PubMedCrossRefGoogle Scholar
  13. Bulf H, Johnson SP, Valenza E (2011) Visual statistical learning in the newborn infant. Cogn 121:127–132. doi: 10.1016/j.cognition.2011.06.010 CrossRefGoogle Scholar
  14. Byrne RMJ (2002) Mental models and counterfactual thoughts about what might have been. Trends Cogn Sci 6:426–431. doi: 10.1016/S1364-6613(02)01974-5 PubMedCrossRefGoogle Scholar
  15. Cassidy TP, Lewis S, Gray CS (1998) Recovery from visuospatial neglect in stroke patients. J Neurol Neurosurg Psychiatry 64:555–557. doi: 10.1136/jnnp.64.4.555 PubMedCentralPubMedCrossRefGoogle Scholar
  16. Chan YC, Chou TL, Chen HC, Liang KC (2012a) Segregating the comprehension and elaboration processing of verbal jokes: an fMRI study. Neuroimage 61:899–906. doi: 10.1016/j.neuroimage.2012.03.052 PubMedCrossRefGoogle Scholar
  17. Chan YC, Chou TL, Chen HC, Yeh YC, Lavallee JP, Liang KC, Chang KE (2012b) Towards a neural circuit model of verbal humor processing: an fMRI study of the neural substrates of incongruity detection and resolution. Neuroimage 66:169–176. doi: 10.1016/j.neuroimage.2012.10.019 CrossRefGoogle Scholar
  18. Christman SD, Henning B, Geers AL, Propper RE, Niebauer CL (2008) Mixed-handed persons are more easily persuaded and are more gullible: interhemispheric interaction and belief updating. Laterality 13:403–426. doi: 10.1080/13576500802079646 PubMedCrossRefGoogle Scholar
  19. Christman SD, Sontam V, Jasper JD (2009) Individual differences in ambiguous-figure perception: degree of handedness and interhemispheric interaction. Percept 38:1183–1198. doi: 10.1068/p6131 CrossRefGoogle Scholar
  20. Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324. doi: 10.1016/j.neuron.2008.04.017 PubMedCentralPubMedCrossRefGoogle Scholar
  21. Craig AD (2009) How do you feel–now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70. doi: 10.1038/nrn2555 PubMedCrossRefGoogle Scholar
  22. Danckert J (in press) Spatial neglect: not simply disordered attention. In: Schweizer T, MacDonald RL (eds) The behavioral consequences of stroke. Springer, New YorkGoogle Scholar
  23. Danckert J, Ferber S, Doherty T, Steinmetz H, Nicolle D, Goodale MA (2002) Selective, non-lateralised impairment of motor imagery following right parietal damage. Neurocase 8:194–204PubMedGoogle Scholar
  24. Danckert J, Ferber S, Pun C, Broderick C, Striemer C, Rock S, Stewart D (2007) Neglected time: impaired temporal perception of multisecond intervals in unilateral neglect. J Cogn Neurosci 19:1706–1720. doi: 10.1162/jocn.2007.19.10.1706 PubMedCrossRefGoogle Scholar
  25. Danckert J, Stöttinger E, Anderson B (2012a) Neglect as a disorder of representational updating. NOVA Open Access, New YorkGoogle Scholar
  26. Danckert J, Stöttinger E, Quehl N, Anderson B (2012b) Right hemisphere brain damage impairs strategy updating. Cereb Cortex 22:2745–2760. doi: 10.1093/cercor/bhr351 PubMedCrossRefGoogle Scholar
  27. Decety J, Lamm C (2007) The role of the right temporoparietal junction in social interaction: how low-level computational processes contribute to meta-cognition. Nerurosci 13:580–593. doi: 10.1177/1073858407304654 Google Scholar
  28. Ferber S, Danckert J (2006) Lost in space: the fate of memory representations for non-neglected stimuli. Neuropsychologia 44:320–325. doi: 10.1016/j.neuropsychologia.2005.04.018 PubMedCrossRefGoogle Scholar
  29. Filipowicz A, Anderson B, Danckert J (2013) Learning what from where: effects of spatial regularity on non-spatial sequence learning and updating. Advanced online publication, Q J Exp Psy. doi: 10.1080/17470218.2013.867518 Google Scholar
  30. Fink GR, Halligan PW, Marshall JC, Frith CD, Frackowiak RS, Dolan RJ (1997) Neural mechanisms involved in the processing of global and local aspects of hierarchically organized visual stimuli. Brain 120:1779–1791. doi: 10.1093/brain/120.10.1779 PubMedCrossRefGoogle Scholar
  31. Fink JN, Selim MH, Kumar S, Voetsch B, Fong WC, Caplan LR (2005) Insular cortex infarction in acute middle cerebral artery territory stroke: predictor of stroke severity and vascular lesion. Arch Neuro 62:1081–1085. doi: 10.1001/archneur.62.7.1081 CrossRefGoogle Scholar
  32. Fischer GH (1967a) Measuring ambiguity. Am J Psychol 80:541–557CrossRefGoogle Scholar
  33. Fischer GH (1967b) Preparation of ambiguous stimulus materials. Percept Psychophys 2:421–422. doi: 10.3758/BF03208780 CrossRefGoogle Scholar
  34. Fiser J, Aslin RN (2002) Statistical learning of new visual feature combinations by infants. Proc Natl Acad Sci USA 99:15822–15826. doi: 10.1073/pnas.232472899 PubMedCentralPubMedCrossRefGoogle Scholar
  35. Gazzaniga MS (1995) Principles of human brain organization derived from split-brain studies. Neuron 14:217–228PubMedCrossRefGoogle Scholar
  36. Griffin R, Friedman O, Ween J, Winner E, Happé F, Brownell H (2006) Theory of mind and the right cerebral hemisphere: refining the scope of impairment. Laterality 11:195–225. doi: 10.1080/13576500500450552 PubMedCrossRefGoogle Scholar
  37. Griffiths TL, Tenenbaum JB (2012) Optimal predictions in everyday cognition. Psychol Sci 17:767–773. doi: 10.1080/13576500500450552 CrossRefGoogle Scholar
  38. Happé F, Brownell H, Winner E (1999) Acquired theory of mind impairments following stroke. Cogn 70:211–240. doi: 10.1016/S0010-0277(99)00005-0 CrossRefGoogle Scholar
  39. Haruno M, Kawato M (2006) Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol 95:948–959. doi: 10.1152/jn.00382.2005 PubMedCrossRefGoogle Scholar
  40. Hohwy J (2012) Attention and conscious perception in the hypothesis testing brain. Conscious Res 3:1–14. doi: 10.3389/fpsyg.2012.00096 Google Scholar
  41. Husain M, Shapiro K, Martin J, Kennard C (1997) Abnormal temporal dynamics of visual attention in spatial neglect patients. Nature 385:154–156. doi: 10.1038/385154a0 PubMedCrossRefGoogle Scholar
  42. Husain M, Mannan S, Hodgson T, Wojciulik E, Driver J, Kennard C (2001) Impaired spatial working memory across saccades contributes to abnormal search in parietal neglect. Brain 124:941–952. doi: 10.1093/brain/124.5.941 PubMedCrossRefGoogle Scholar
  43. Jastrow J (1900) Fact and fable in psychology. Houghton Mifflin, BostonCrossRefGoogle Scholar
  44. Jenkinson M, Pechaud M, Smith S (2005) BET2: MR-based estimation of brain, skull and scalp surfaces. In: Eleventh annual meeting of the organization for human brain mappingGoogle Scholar
  45. Jones CL, Ward J, Critchley HD (2010) The neuropsychological impact of insular cortex lesions. J Neurol Neurosurg Psychiatry 81:611–618. doi: 10.1136/jnnp.2009.193672 PubMedCrossRefGoogle Scholar
  46. Kleinschmidt A, Büchel C, Zeki S, Frackowiak RSJ (1998) Human brain activity during spontaneously reversing perception of ambiguous figures. Proc R Soc Lond Ser B Biol Sci 265:2427–2433. doi: 10.1098/rspb1998.0594 CrossRefGoogle Scholar
  47. Long GM, Toppino TC (2004) Enduring interest in perceptual ambiguity: alternating views of reversible figures. Psychol Bull 130:748. doi: 10.1037/0033-2909.130.5.748 PubMedCrossRefGoogle Scholar
  48. Lumer ED, Friston KJ, Rees G (1998) Neural correlates of perceptual rivalry in the human brain. Science 280:1930–1934. doi: 10.1126/science.280.5371.1930 PubMedCrossRefGoogle Scholar
  49. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667. doi: 10.1007/s00429-010-0262-0 PubMedCentralPubMedCrossRefGoogle Scholar
  50. Merrifield C, Hurwitz M, Danckert J (2010) Multimodal temporal perception deficits in a patient with left spatial neglect. Cogn Neurosci 1:244–253. doi: 10.1080/17588921003759934 PubMedCrossRefGoogle Scholar
  51. Miller MB, Valsangkar-Smith M, Newman S, Dumont H, Wolford G (2005) Brain activations associated with probability matching. Neuropsychologia 43:1598–1608. doi: 10.1016/j.neuropsychologia.2005.01.021 PubMedCrossRefGoogle Scholar
  52. Mitchell JP (2008) Activity in right temporo-parietal junction is not selective for theory-of-mind. Cereb Cortex 18:262–271. doi: 10.1093/cercor/bhm051 PubMedCrossRefGoogle Scholar
  53. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The montreal cognitive assessment, moca: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699. doi: 10.1111/j.1532-5415.2005.53221.x PubMedCrossRefGoogle Scholar
  54. Nelson HE (1976) A modified card sorting test sensitive to frontal lobe defects. Cortex 12:313–324. doi: 10.1016/S0010-9452(76)80035-4 PubMedCrossRefGoogle Scholar
  55. Nijboer T, Van de Port I, Schepers V, Post M, Visser-Meily A (2013) Predicting functional outcome after stroke: the influence of neglect on basic activities in daily living. Front hum neurosci 7. doi: 10.3389/fnhum.2013.00182
  56. Peirce JW (2009) Generating stimuli for neuroscience using PsychoPy. Front Neuroinform 2:1–8. doi: 10.3389/neuro.11.010.2008 Google Scholar
  57. Perner J (1991) Understanding the representational mind. Learning development and conceptual change. The MIT Press, CambridgeGoogle Scholar
  58. Perner J, Aichhorn M, Kronbichler M, Staffen W, Ladurner G (2006) Thinking of mental and other representations: the roles of left and right temporo-parietal junction. Soc Neurosci 1:245–258. doi: 10.1080/17470910600989896 PubMedCrossRefGoogle Scholar
  59. Piper BJ, Li V, Eiwaz MA, Kobel YV, Benice TS, Chu AM, Olsen RHJ, Rice DZ, Gray HM, Mueller ST (2011) Executive function on the psychology experiment building language tests. Behav Res Methods 44:110–123. doi: 10.3758/s13428-011-0096-6 CrossRefGoogle Scholar
  60. Rafetseder E, Perner J (2010) Is reasoning from counterfactual antecedents evidence for counterfactual reasoning? Think Reason 16:131–155. doi: 10.1080/13546783.2010.488074 PubMedCentralPubMedCrossRefGoogle Scholar
  61. Ramachandran VS (1995) Anosognosia in parietal lobe syndrome. Conscious Cogn 4:22–51. doi: 10.1006/ccog.1995.1002 PubMedCrossRefGoogle Scholar
  62. Rauch SL, Savage CR, Brown HD, Curran T, Alpert NM, Kendrick A, Fischman AJ, Kosslyn SM (1995) A PET investigation of implicit and explicit sequence learning. Hum Brain Mapp 3:271–286. doi: 10.1002/hbm.460030403 CrossRefGoogle Scholar
  63. Ringman JM, Saver JL, Woolson RF, Clarke WR, Adams HP (2004) Frequency, risk factors, anatomy, and course of unilateral neglect in an acute stroke cohort. Neurology 63:468–474. doi: 10.1212/01.WNL.0000133011.10689.CE PubMedCrossRefGoogle Scholar
  64. Robertson LC, Delis DC (1986) ‘Part-whole’processing in unilateral brain-damaged patients: dysfunction of hierarchical organization. Neuropsychologia 24:363–370. doi: 10.1016/0028-3932(86)90021-7 PubMedCrossRefGoogle Scholar
  65. Roser ME, Fiser J, Aslin RN, Gazzaniga MS (2011) Right hemisphere dominance in visual statistical learning. J Cogn Neurosci 23:1088–1099. doi: 10.1162/jocn.2010.21508 PubMedCentralPubMedCrossRefGoogle Scholar
  66. Samson AC, Zysset S, Huber O (2008) Cognitive humor processing: different logical mechanisms in nonverbal cartoons—an fMRI study. Soc Neurosci 3:125–140. doi: 10.1080/17470910701745858 PubMedCrossRefGoogle Scholar
  67. Sato Y, Akiyama E, Farmer JD (2002) Chaos in learning a simple two-person game. Proc Natl Acad Sci 99:4748–4751. doi: 10.1073/pnas.032086299 PubMedCentralPubMedCrossRefGoogle Scholar
  68. Seger CA, Prabhakaran V, Poldrack RA, Gabrieli JD (2000) Neural activity differs between explicit and implicit learning of artificial grammar strings: an fMRI study. Psychobiology 28:283–292Google Scholar
  69. Seger CA, Peterson EJ, Cincotta CM, Lopez-Paniagua D, Anderson CW (2010) Dissociating the contributions of independent corticostriatal systems to visual categorization learning through the use of reinforcement learning modeling and Granger causality modeling. Neuroimage 50:644–656. doi: 10.1016/j.neuroimage.2009.11.083 PubMedCentralPubMedCrossRefGoogle Scholar
  70. Shapiro K, Hillstrom AP, Husain M (2002) Control of visuotemporal attention by inferior parietal and superior temporal cortex. Curr Biol 12:1320–1325. doi: 10.1016/S0960-9822(02)01040-0 PubMedCrossRefGoogle Scholar
  71. Shaqiri A, Anderson B (2013) Priming and statistical learning in right brain damage patients. Neuropsychologia 51:2526–2533PubMedCrossRefGoogle Scholar
  72. Shaqiri A, Anderson B, Danckert J (2013) Statistical learning as a tool for rehabilitation in spatial neglect. Front hum neurosci, 7. doi: 10.3389/fnhum.2013.00224
  73. Spinazzola L, Pia L, Folegatti A, Marchetti C, Berti A (2008) Modular structure of awareness for sensorimotor disorders: evidence from anosagnosia for hemiplegia and anosagnosia for hemianaesthesia. Neuropsychologia 46:915–926. doi: 10.1016/j.neuropsychologia.2007.12.015 PubMedCrossRefGoogle Scholar
  74. Stöttinger E, Filipowicz A, Anderson B, Danckert J (2012) Hemispheric effects on strategy updating. Poster presented at the CNS (Cognitive Neuroscience Society), Chicago, USAGoogle Scholar
  75. Stöttinger E, Filipowicz A, Danckert J, Anderson B (in press) The effects of prior learned strategies on updating an opponent’s strategy in the rock, paper, scissors game. Cogn Sci. doi: 10.1111/cogs.12115
  76. Striemer C, Ferber S, Danckert J (2013) Can spatial working memory training rehabilitate neglect? Front in hum neurosci. doi: 10.3389/fnhum.2013.00334 Google Scholar
  77. Tenenbaum JB, Kemp C, Griffiths TL, Goodman ND (2011) How to grow a mind: statistics, structure, and abstraction. Science 331:1279–1285. doi: 10.1126/science.1192788 PubMedCrossRefGoogle Scholar
  78. Turk-Browne NB, Scholl BJ, Chun MM, Johnson MK (2009) Neural evidence of statistical learning: efficient detection of visual regularities without awareness. J Cogn Neurosci 21:1934–1945. doi: 10.1162/jocn.2009.21131 PubMedCentralPubMedCrossRefGoogle Scholar
  79. Vickery TJ, Jiang YV (2009) Inferior parietal lobule supports decision making under uncertainty in humans. Cereb Cortex 19:916–925. doi: 10.1093/cercor/bhn140 PubMedCrossRefGoogle Scholar
  80. Vocat R, Saj A, Vuilleumier P (2012) The riddle of anosognosia: does unawareness of hemiplegia involve a failure to update beliefs? Cortex. doi: 10.1016/j.cortex.2012.10.009 PubMedGoogle Scholar
  81. Vogeley K, Bussfeld P, Newen A, Herrmann S, Happé F, Falkai P, Maier W, Shah NJ, Fink GR, Zilles K (2001) Mind reading: neural mechanisms of theory of mind and self-perspective. Neuroimage 14:170–181. doi: 10.1006/nimg.2001.0789 PubMedCrossRefGoogle Scholar
  82. Wilson B, Cockburn J, Halligan P (1987) Development of a behavioural test of visuospatial neglect. Arch Phys Med Rehabil 68:98–102PubMedGoogle Scholar
  83. Winner E, Brownell H, Happé F, Blum A, Pincus D (1998) Distinguishing lies from jokes: theory of mind deficits and discourse interpretation in right hemisphere brain-damaged patients. Brain Lang 62:89–106. doi: 10.1006/brln.1997.1889 PubMedCrossRefGoogle Scholar
  84. Wolford G, Miller MB, Gazzaniga M (2000) The left hemisphere’s role in hypothesis formation. J Neurosci 20:RC64PubMedGoogle Scholar
  85. Wolford G, Newman SE, Miller MB, Wig GS (2004) Searching for patterns in random sequences. Can J Exp Psychol 58:221–228. doi: 10.1037/h0087446 PubMedCrossRefGoogle Scholar
  86. Zaretskaya N, Thielscher A, Logothetis NK, Bartels A (2010) Disrupting parietal function prolongs dominance durations in binocular rivalry. Curr Biol 20:2106–2111. doi: 10.1016/j.cub.2010.10.046 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Elisabeth Stöttinger
    • 1
  • Alex Filipowicz
    • 1
  • Elahe Marandi
    • 1
  • Nadine Quehl
    • 1
  • James Danckert
    • 1
  • Britt Anderson
    • 1
    • 2
  1. 1.Department of PsychologyUniversity of WaterlooWaterlooCanada
  2. 2.Centre for Theoretical NeuroscienceUniversity of WaterlooWaterlooCanada

Personalised recommendations