Learned Irrelevance Revisited: Pathology-Based Individual Differences, Normal Variation and Neural Correlates

  • Aleksandra GruszkaEmail author
  • Adam Hampshire
  • Adrian M. Owen
Part of the The Springer Series on Human Exceptionality book series (SSHE)


The function of the human executive system can broadly be described as the seeking out and processing of those signals and memories that are of the greatest relevance when guiding deliberate and adaptive behaviours. This task is not easy, however, since it requires almost constant shifting of attention in response to irregular alterations in the contingencies relating stimuli, responses, and environmental feedback. An individual’s current belief regarding these contingencies guides response within a given context, and the representation of this belief and its consequent behaviour is often referred to as an “attentional set”. Consequently, attentional set-shifting is an important executive function responsible for altering a behavioural response in reaction to the changing contingencies (Cools, Barker, Sahakian, & Robbins, 2001; Gotham, Brown, & Marsden, 1986). Such flexibility underlies a wide range of behaviours: the better the set-shifting capacity, the more flexible the person is at adapting to change. At the other end of this continuum are many psychiatric groups, neurodegenerative groups and even healthy elderly and young subjects that have been shown repeatedly to be impaired in attentional set-shifting performance. One specific form of these impairments lies in an inability to attend to, or to learn about, information which has previously been shown to be irrelevant. This phenomenon called learned irrelevance (LI) (Mackintosh, 1973) is very mysterious, because unlike other aspects of attentional set-shifting, it appears to be neither dependent on the frontal lobe (e.g. Owen et al., 1993) nor affected by dopamine (Owen et al., 1993; Słabosz et al., 2006), and, therefore, may not be coded for in the parts of the brain that are typically considered “executive” at all.


Conditioned Stimulus Frontal Lobe Anterior Cingulate Cortex Unconditioned Stimulus Latent Inhibition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Agid, Y., Javoy Agid, F., & Ruberg, M. (1987). Biochemistry of neurotransmitters in Parkinson’s disease. In C. D. Marsden & S. Fahn (Eds.), Movement disorders (Vol. 2, pp. 166–230). London: Butterworth.Google Scholar
  2. Alexander, G. E., Delong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–381.PubMedCrossRefGoogle Scholar
  3. Anderson, C. V., Bigler, E. D., & Blatter, D. D. (1995). Frontal lobe lesions, diffuse damage, and neuropsychological functioning in traumatic brain-injured patients. Journal of Clinical and Experimental Neuropsychology, 17(6), 900–908.PubMedCrossRefGoogle Scholar
  4. Anderson, S. V., Damasio, H., Jones, R. D., & Tranel, D. (1991). Wisconsin card sorting test performance as a measure of frontal lobe damage. Journal of Clinical and Experimental Neuropsychology, 13(6), 909–922.PubMedCrossRefGoogle Scholar
  5. Aron, A. R. (2008). Progress in executive-function research. From tasks to functions to regions to networks. Current Directions in Psychological Science, 17(2), 124–129.CrossRefGoogle Scholar
  6. Baker, A. G., & Mackintosh, N. J. (1979). Preexposure to the CS alone, US alone, or CS and US uncorrelated: Latent inhibition, blocking by context or learned irrelevance? Learning and Motivation, 10(3), 278–294.CrossRefGoogle Scholar
  7. Barcelo, F., & Santome-Calleja, A. (2000). A critical review of the specificity of the Wisconsin card sorting test for the assessment of prefrontal function. Revista de Neurologia, 30, 855–864.PubMedGoogle Scholar
  8. Barcelo, F., Sanz, M., Molina, V., & Rubia, J. F. (1997). The Wisconsin card sorting test and the assessment of frontal function: A validation study with event-related potentials. Neuropsychologia, 35, 399–408.PubMedCrossRefGoogle Scholar
  9. Bennett, C. H., Wills, S. J., Oakeshott, S. M., & Mackintosh, N. J. (2000). Is the context specificity of latent inhibition a sufficient explanation of learned irrelevance? The Quarterly Journal of Experimental Psychology. B, Comparative and Physiological Psychology, 53(3), 239–253.PubMedGoogle Scholar
  10. Bonardi, C., & Hall, G. (1996). Learned irrelevance: No more than the sum of CS and US preexposure effects? Journal of Experimental Psychology: Animal Behavior Processes, 22(2), 183–191.CrossRefGoogle Scholar
  11. Canavan, A. G. M., Passingham, R. E., Marsden, C. D., Quinn, N., Wyke, M., & Polkey, C. E. (1989). The performance on learning tasks of patients in the early stages of Parkinson’s disease. Neuropsychologia, 27, 141–156.PubMedCrossRefGoogle Scholar
  12. Cools, R., Barker, R. A., Sahakian, B. J., & Robbins, T. W. (2001). Mechanisms of cognitive set flexibility in Parkinson’s disease. Brain, 124, 2503–2512.PubMedCrossRefGoogle Scholar
  13. Cools, A. R., van den Bercken, J. H., Horstink, M. W., van Spaendonck, K. P., & Berger, H. J. (1984). Cognitive and motor shifting aptitude disorder in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 47(5), 443–453.PubMedCrossRefGoogle Scholar
  14. Cooper, J. A., Sagar, H. J., Jordan, N., Harvey, N. S., & Sullivan, E. V. (1991). Cognitive impairment in early, untreated Parkinson’s disease and its relationship to motor disability. Brain, 114, 2095–2122.PubMedCrossRefGoogle Scholar
  15. Demakis, G. J. (2003). A meta-analytic review of the sensitivity of the Wisconsin card sorting test to frontal and lateralized frontal brain damage. Neuropsychology, 17(2), 255–264.PubMedCrossRefGoogle Scholar
  16. Dias, R., Robbins, T. W., & Roberts, A. C. (1996). Dissociation in prefrontal cortex of affective and attentional shifts. Nature, 380, 69–72.PubMedCrossRefGoogle Scholar
  17. Dias, R., Robbins, T. W., & Roberts, A. C. (1997). Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin card sort test: Restriction to novel situations and independence from ‘on-line’ processing. Journal of Neuroscience, 17(23), 9285–9297.PubMedGoogle Scholar
  18. Downes, J. J., Roberts, A. C., Sahakian, B. J., Evenden, J. L., Morris, R. G., & Robbins, T. W. (1989). Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson’s disease: Evidence for a specific attentional dysfunction. Neuropsychologia, 27(11–12), 1329–1343.PubMedCrossRefGoogle Scholar
  19. Drewe, E. A. (1974). The effect of type and area of brain lesion on Wisconsin card sorting test performance. Cortex, 10(2), 159–170.PubMedGoogle Scholar
  20. Eslinger, P. J., & Damasio, A. R. (1985). Severe disturbance of higher cognition after bilateral frontal lobe ablation patient EVR. Neurology, 35, 1731–1741.PubMedCrossRefGoogle Scholar
  21. Fellows, L. K., & Farah, M. J. (2003). Ventromedial frontal cortex mediates affective shifting in humans: Evidence from a reversal learning paradigm. Brain, 126, 1830–1837.PubMedCrossRefGoogle Scholar
  22. Flowers, K. A., & Robertson, C. (1985). The effect of Parkinson’s disease on the ability to maintain a mental set. Journal of Neurology, Neurosurgery, and Psychiatry, 48, 517–529.PubMedCrossRefGoogle Scholar
  23. Foldi, N. S., Helm-Estabrooks, N., Redfield, J., & Nickel, D. G. (2003). Perseveration in normal aging: A comparison of perseveration rates on design fluency and verbal generative tasks. Aging, Neuropsychology, and Cognition, 10(4), 268–280.CrossRefGoogle Scholar
  24. Fork, M., Bartels, C., Ebert, A. D., Grubich, C., Synowitz, H., & Wallesch, C. W. (2005). Neuropsychological sequelae of diffuse traumatic brain injury. Brain Injury, 19(2), 101–108.PubMedCrossRefGoogle Scholar
  25. Gal, G., Mendlovic, S., Bloch, Y., Beitler, G., Levkovitz, Y., Young, A. M. J., et al. (2005). Learned irrelevance is disrupted in first-episode but not chronic schizophrenia patients. Behavioural Brain Research, 159(2), 267–275.PubMedCrossRefGoogle Scholar
  26. Gauntlett-Gilbert, J., Roberts, R. C., & Brown, V. J. (1999). Mechanisms underlying attentional set-shifting in Parkinson’s disease. Neuropsychologia, 37(5), 605–616.PubMedCrossRefGoogle Scholar
  27. Gluck, M., & Myers, C. (1993). Hippocampal mediation of stimulus representation: A computational theory. Hippocampus, 3, 491–516.PubMedCrossRefGoogle Scholar
  28. Gotham, A.-M., Brown, R. G., & Marsden, C. D. (1986). Levodopa treatment may benefit or impair frontal function in Parkinson’s disease. The Lancet, 328(8513), 970–971.CrossRefGoogle Scholar
  29. Grant, D. A., & Berg, E. A. (1948). A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. Journal of Experimental Psychology, 38, 404–411.PubMedCrossRefGoogle Scholar
  30. Gray, J. A., Joseph, M. H., Hemsley, D. R., Young, A. M. J., Warburton, E. C., Boulenguez, P., et al. (1995). The role of mesolimbic dopaminergic and retrohippocampal afferents to the nucleus accumbens in latent inhibition: implications for schizophrenia. Behavioural Brain Research, 71, 19–31.PubMedCrossRefGoogle Scholar
  31. Gray, J. A., Moran, P. M., Grigoryan, G. A., Peters, S. L., Young, A. M. J., & Joseph, M. H. (1997). Latent inhibition: The nucleus accumbens connection revisited. Behavioural Brain Research, 88, 27–34.PubMedCrossRefGoogle Scholar
  32. Gruszka, A., Hampshire, A., & Owen, A. M. (in prep.). Contrasting cortical and subcortical activations produced by learned irrelevance and perseveration.Google Scholar
  33. Hampshire, A., Gruszka, A., Fallon, S. J., & Owen, A. M. (2008). Inefficiency in self-organised attentional switching in the normal ageing population is associated with decreased activity in the ventrolateral prefrontal cortex. Journal of Cognitive Neuroscience, 20, 1670–1686.PubMedCrossRefGoogle Scholar
  34. Hampshire, A., & Owen, A. M. (2006). Fractionating attentional control using event-related fMRI. Cerebral Cortex, 16(12), 1679–1689.PubMedCrossRefGoogle Scholar
  35. Hermann, B. P., Wyler, A. R., & Richey, E. T. (1988). Wisconsin card sorting test performance in patients with complex partial seizures of temporal-lobe origin. Journal of Clinical and Experimental Neuropsychology, 10(4), 467–476.PubMedCrossRefGoogle Scholar
  36. Honey, R. C., & Good, M. (1993). Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. Behavioral Neuroscience, 107, 23–33.PubMedCrossRefGoogle Scholar
  37. Horner, M. D., Flashman, L. A., Freides, D., Epstein, C. M., & Bakay, R. A. (1996). Temporal lobe epilepsy and performance on the Wisconsin card sorting test. Journal of Clinical and Experimental Neuropsychology, 18(2), 310–313.PubMedCrossRefGoogle Scholar
  38. Jones, B., & Mishkin, M. (1972). Limbic lesions and the problem of stimulus-reinforcement associations. Experimental Neurology, 36, 362–377.PubMedCrossRefGoogle Scholar
  39. Joseph, M. H., Peters, S. L., Moran, P. M., Grigoryan, G. A., Young, A. M. J., & Gray, J. A. (2000). Modulation of latent inhibition in the rat by altered dopamine transmission in the nucleus accumbens at the time of conditioning. Neuroscience, 101, 921–930.PubMedCrossRefGoogle Scholar
  40. Lubow, R. E. (1973). Latent inhibition. Psychological Bulletin, 79(6), 398–407.PubMedCrossRefGoogle Scholar
  41. Lubow, R. E. (1989). Latent inhibition and conditioned attention theory. New York: Cambridge Uniersity Press.CrossRefGoogle Scholar
  42. Lubow, R. E., Dressler, R., & Kaplan, O. (1999). The effects of target and distractor familiarity on visual search in de novo Parkinson’s disease patients: Latent inhibition and novel pop-out. Neuropsychology, 13(3), 415–423.PubMedCrossRefGoogle Scholar
  43. Mackintosh, N. J. (1973). Stimulus selection: Learning to ignore stimuli that predict no change in reinforcement. In R. A. Hinde & J. S. Hinde (Eds.), Constraints on learning (pp. 75–96). London: Academic Press.Google Scholar
  44. Mackintosh, N. J. (1983). Conditioning and associative learning. Oxford: The Clarenden Press.Google Scholar
  45. Maes, J. H. R., Damen, M. D. C., & Eling, P. A. T. M. (2004). More learned irrelevance than perseveration errors in rule shifting in healthy subjects. Brain and Cognition, 54, 201–211.PubMedCrossRefGoogle Scholar
  46. Maes, J. H. R., Vich, J., & Eling, P. A. (2006). Learned irrelevance and perseveration in a total change dimensional shift task. Brain and Cognition, 62(1), 74–79.PubMedCrossRefGoogle Scholar
  47. Matzel, L. D., Schachtman, T. R., & Miller, R. R. (1988). Learned irrelevance exceeds the sum of CS-Preexposure and US-Preexposure deficits. Journal of Experimental Psychology: Animal Behavior Processes, 14(3), 311–319.CrossRefGoogle Scholar
  48. Milner, B. (1963). Effects of different brain lesions on card sorting. Archives of Neurology, 9, 90–100.CrossRefGoogle Scholar
  49. Mountain, M. A., & Snow, W. G. (1993). Wisconsin card sorting test as a measure of frontal pathology: A review. Clinical Neuropsychology, 7, 108–118.CrossRefGoogle Scholar
  50. Nagahama, Y., Okina, T., Suzuki, N., Nabatame, H., & Matsuda, M. (2005). The cerebral correlates of different types of perseveration in the Wisconsin card sorting test. Journal of Neurology, Neurosurgery and Psychiatry, 76, 169–175.CrossRefGoogle Scholar
  51. Nakahara, K., Hayashi, T., Konishi, S., & Miyashita, Y. (2002). Functional MRI of macaque monkeys performing a cognitive set-shifting task. Science, 295, 1532–1536.PubMedCrossRefGoogle Scholar
  52. Owen, A. M., James, M., Leigh, P. N., Summers, B. A., Marsden, C. D., Quinn, N. P., et al. (1992). Fronto-striatal cognitive deficits at different stages of Parkinson’s disease. Brain: A Journal of Neurology, 115(6), 1727–1751.CrossRefGoogle Scholar
  53. Owen, A. M., Roberts, A. C., Hodges, J. R., Summers, B. A., Polkey, C. E., & Robbins, T. W. (1993). Contrasting mechanisms of impaired attentional set-shifting in patients with frontal lobe damage or Parkinson’s disease. Brain: A Journal of Neurology, 116(5), 1159–1175.CrossRefGoogle Scholar
  54. Owen, A. M., Roberts, A. C., Polkey, C. E., Sahakian, B. J., & Robbins, T. W. (1991). Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in Man. Neuropsychologia, 29, 993–1006.PubMedCrossRefGoogle Scholar
  55. Reitan, R. M., & Wolfson, D. (1994). A selective and critical review of neuropsychological deficits and the frontal lobes. Neuropsychology Review, 4, 161–198.PubMedCrossRefGoogle Scholar
  56. Ridderinkhof, K. R., Span, M. M., & van der Molen, M. W. (2002). Perseverative behavior and adaptive control in older adults: Performance monitoring, rule induction, and set shifting. Brain and Cognition, 49, 382–401.PubMedCrossRefGoogle Scholar
  57. Roberts, A. C., De Salvia, M. A., Wilkinson, L. S., Collins, P., Muir, J. L., Everitt, B. J., et al. (1994). 6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin card sort test: Possible interactions with subcortical dopamine. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 14(5, Part 1), 2531–2544.Google Scholar
  58. Roberts, A. C., Robbins, T. W., & Everitt, B. J. (1988). The effects of intradimensional and extradimensional shifts on visual discrimination learning in humans and non-human primates. Quarterly Journal of Experimental Psychology, 40B, 321–341.Google Scholar
  59. Rogers, R. D., Andrews, T. C., Grasby, P. M., Brooks, D. J., & Robbins, T. W. (2000). Contrasting cortical and subcortical activations produced by attentional-set shifting and reversal learning in humans. Journal of Cognitive Neuroscience, 12, 142–162.PubMedCrossRefGoogle Scholar
  60. Sahakian, B. J., Downes, J. J., Eagger, S., & Evenden, J. L., et al. (1990). Sparing of attentional relative to mnemonic function in a subgroup of patients with dementia of the Alzheimer type. Neuropsychologia, 28(11), 1197–1213.PubMedCrossRefGoogle Scholar
  61. Słabosz, A., Lewis, S. J. G., Śmigasiewicz, K., Szymura, B., Barker, R. A., & Owen, A. M. (2006). The role of learned irrelevance in attentional set-shifting impairments in Parkinson’s disease. Neuropsychology, 20(5), 578–588.PubMedCrossRefGoogle Scholar
  62. Stuss, D. T., & Benson, D. F. (1984). Neuropsychological studies of the frontal lobes. Psychological Bulletin, 95(1), 3–28.PubMedCrossRefGoogle Scholar
  63. Taylor, A. E., Saint-Cyr, J. A., & Lang, A. E. (1986). Frontal lobe disfunction in Parkinson’s disease. Brain, 109, 845–883.PubMedCrossRefGoogle Scholar
  64. Tsuchiya, H., Yamaguchi, S., & Kobayashi, S. (2000). Impaired novelty detection and frontal lobe dysfunction in Parkinson’s disease. Neuropsychologia, 38(5), 645–654.PubMedCrossRefGoogle Scholar
  65. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273–89.PubMedCrossRefGoogle Scholar
  66. van Spaendonck, K. P. M., Berger, H. J. C., Horstink, M. W. I. M., Borm, G. F., & Cools, A. R. (1995). Card sorting performance in Parkinson’s disease: A comparison between acquisition and shifting performance. Journal of Clinical and Experimental Neuropsychology, 17(6), 918–925.PubMedCrossRefGoogle Scholar
  67. van Spaendonck, K. P. M., Berger, H. J. C., Horstink, M. W. I. M., Buytenhuijs, E. L., & Cools, A. R. (1996). Executive functions and disease characteristics in Parkinson’s disease. Neuropsychologia, 34(7), 617–626.PubMedCrossRefGoogle Scholar
  68. Weiner, I., & Feldon, J. (1997). The switching model of latent inhibition: An update of neural substrates. Behavioural Brain Research, 88, 11–25.PubMedCrossRefGoogle Scholar
  69. Young, A. M. J., Kumari, V., Mehrotra, R., Hemsley, D. R., Andrew, C., Sharma, T., Williams, S. C. R., & Gray, J. A., (2005). Disruption of learned irrelevance in acute schizophrenia in a novel continuous within-subject paradigm suitable for fMRI. Behavioural Brain Research, 156(2), 277–288.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Aleksandra Gruszka
    • 1
    Email author
  • Adam Hampshire
    • 2
  • Adrian M. Owen
    • 2
  1. 1.Institute of Psychology, Jagiellonian UniversityCracowPoland
  2. 2.MRC Cognition and Brain Sciences UnitCambridgeUK

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