Hallucinations as Top-Down Effects on Perception

Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

Volumn 1, Issue 5, 2016, Pages 393-400

  Powers, Albert R ^a   Kelley, Megan ^a   Corlett, Philip R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Connectivity; Hallucinations; Modularity; Neuroimaging; Neuropsychology; Predictive coding; Psychosis

Indexed keywords

COGNITION; HALLUCINATION; HUMAN; MENTAL DISEASE; NERVE CELL NETWORK; NEUROIMAGING; NEUROSCIENCE; PERCEPTION; PRIORITY JOURNAL; REVIEW;

EID: 84995610522     PISSN: 24519022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpsc.2016.04.003     Document Type: Review

References (123)

1. 1 Jenkin, Z., Siegel, S., Cognitive penetrability: Modularity, epistemology, and ethics. Rev Philosophy Psychol, 6, 2015 pp.
2. 2 Firestone, C., Scholl, B.J., Cognition does not affect perception: Evaluating the evidence for ‘top-down’ effects. Behav Brain Sci, 2015, 1–77.
3. 3 Fodor, J.A., The Modularity of Mind: An Essay on Faculty Psychology. 1983, MIT Press, Cambridge, Massachusetts.
4. 4 Twyman, A.D., Newcombe, N.S., Five reasons to doubt the existence of a geometric module. Cogn Sci 34 (2010), 1315–1356.
5. 5 Coltheart, M., Brain imaging, connectionism, and cognitive neuropsychology. Cogn Neuropsychol 21 (2004), 21–25.
6. 6 Coltheart, M., Davies, M., Pathologies of Belief. 2000, Blackwell, Oxford.
7. 7 Fotopoulou, A., Time to get rid of the ‘Modular’ in neuropsychology: A unified theory of anosognosia as aberrant predictive coding. J Neuropsychol 8 (2014), 1–19.
8. 8 Catani, M., Ffytche, D.H., The rises and falls of disconnection syndromes. Brain 128 (2005), 2224–2239.
9. 9 Seghier, M.L., Zeidman, P., Neufeld, N.H., Leff, A.P., Price, C.J., Identifying abnormal connectivity in patients using dynamic causal modeling of FMRI responses. Front Syst Neurosci, 4, 2010.
10. 10 Ween, J.E., Functional imaging of stroke recovery: An ecological review from a neural network perspective with an emphasis on motor systems. J Neuroimaging 18 (2008), 227–236.
11. 11 Lupyan, G., Cognitive penetrability of perception in the age of prediction: Predictive systems are penetrable systems. Rev Philosophy Psychol, 2015.
12. 12 Quine, W.V., Quine, W.V., Two dogmas of empiricism. Philosophic Rev, 60, 1951.
13. 13 McKay, R.T., Dennett, D.C., The evolution of misbelief. Behav Brain Sci 32 (2009), 493–510.
14. 14 Johnson, D.D., Fowler, J.H., The evolution of overconfidence. Nature 477 (2011), 317–320.
15. 15 Hume, D., An Enquiry Concerning Human Understanding. 1900, The Open Court Publishing Co, Chicago, Illinois.
16. 16 Helmholtz, H.V., Handbuch der physiologischen Optik. 1867, Voss, Leipzig, Germany.
17. 17 Feldman, H., Friston, K.J., Attention, uncertainty, and free-energy. Front Hum Neurosci, 4, 2010, 215.
18. 18 Friston, K., Kiebel, S., Predictive coding under the free-energy principle. Philosophi Trans R Soc London Series B, Biologic Sci 364 (2009), 1211–1221.
19. 19 Friston, K.J., Stephan, K.E., Free-energy and the brain. Synthese 159 (2007), 417–458.
20. 20 Teufel, C., Subramaniam, N., Fletcher, P.C., The role of priors in Bayesian models of perception. Front Comput Neurosci, 7, 2013, 25.
21. 21 McClelland, J.L., Rumelhart, D.E., An interactive activation model of context effects in letter perception: I. An account of basic findings. Psychologic Rev, 88, 1981 pp.
22. 22 Rumelhart, D.E., McClelland, J.L., An interactive activation model of context effects in letter perception: II. The contextual enhancement effect and some tests and extensions of the model. Psychologic Rev, 89, 1982 pp.
23. 23 Rao, R.P., Ballard, D.H., Predictive coding in the visual cortex: A functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2 (1999), 79–87.
24. 24 Maia, T.V., Cleeremans, A., Consciousness: Converging insights from connectionist modeling and neuroscience. Trends Cogn Sci 9 (2005), 397–404.
25. 25 Friston, K., A theory of cortical responses. Philosophic Trans R Soc London Series B, Biologic Sci 360 (2005), 815–836.
26. 26 Friston, K., Hallucinations and perceptual inferences. Behav Brain Sci 28 (2005), 764–766.
27. 27 Lupyan, G., Swingley, D., Self-directed speech affects visual search performance. Q J Exp Psychol (Hove) 65 (2012), 1068–1085.
28. 28 Lupyan, G., Spivey, M.J., Perceptual processing is facilitated by ascribing meaning to novel stimuli. Curr Biol 18 (2008), R410–R412.
29. 29 Lupyan, G., The conceptual grouping effect: Categories matter (and named categories matter more). Cognition 108 (2008), 566–577.
30. 30 Lupyan, G., Spivey, M.J., Making the invisible visible: Verbal but not visual cues enhance visual detection. PloS One, 5, 2010, e11452.
31. 31 Dikker, S., Rabagliati, H., Farmer, T.A., Pylkkanen, L., Early occipital sensitivity to syntactic category is based on form typicality. Psychol Sci 21 (2010), 629–634.
32. 32 Dikker, S., Rabagliati, H., Pylkkanen, L., Sensitivity to syntax in visual cortex. Cognition 110 (2009), 293–321.
33. 33 Jordan, T.R., Sheen, M., AlJassmi, M.A., Paterson, K.B., A new demonstration of the illusory letters phenomenon: Graphemic restoration in Arabic word perception. Perception 44 (2015), 215–218.
34. 34 Jordan, T.R., Thomas, S.M., Scott-Brown, K.C., The illusory-letters phenomenon: An illustration of graphemic restoration in visual word recognition. Perception 28 (1999), 1413–1416.
35. 35 Lupyan, G., Thompson-Schill, S.L., The evocative power of words: activation of concepts by verbal and nonverbal means. J Exp Psychol Gen 141 (2012), 170–186.
36. 36 den Ouden, H.E., Friston, K.J., Daw, N.D., McIntosh, A.R., Stephan, K.E., A dual role for prediction error in associative learning. Cereb Cortex 19 (2009), 1175–1185.
37. 37 Knill, D.C., Pouget, A., The Bayesian brain: The role of uncertainty in neural coding and computation. Trends Neurosci 27 (2004), 712–719.
38. 38 Swets, J., Tanner, W.P. Jr, Birdsall, T.G., Decision processes in perception. Psychol Rev 68 (1961), 301–340.
39. 39 Scharf, B., Quigley, S., Aoki, C., Peachey, N., Reeves, A., Focused auditory attention and frequency selectivity. Percept Psychophysics 42 (1987), 215–223.
40. 40 Marks, L.E., Wheeler, M.E., Attention and the detectability of weak taste stimuli. Chem Senses 23 (1998), 19–29.
41. 41 Esquirol, J., Hallucinations: Dictionnaire des Sciences Médicales. 1814, CLF Panckouche, París, 1822.
42. 42 Bleuler, E., Lehrbuch der psychiatrie. 2013, Springer-Verlag.
43. 43 Winokur, G., Scharfetter, C., Angst, J., The diagnostic value in assessing mood congruence in delusions and hallucinations and their relationship to the affective state. Eur Arch Psychiatry Neurol Sci 234 (1985), 299–302.
44. 44 Schneider, F., Gur, R.C., Gur, R.E., Shtasel, D.L., Emotional processing in schizophrenia: Neurobehavioral probes in relation to psychopathology. Schizophr Res 17 (1995), 67–75.
45. 45 Olson, P.R., Suddeth, J.A., Peterson, P.J., Egelhoff, C., Hallucinations of widowhood. J Am Geriatr Soc 33 (1985), 543–547.
46. 46 Dewi Rees, W., The hallucinations of widowhood. Br Med J 4 (1971), 37–41.
47. 47 Baethge, C., Grief hallucinations: True or pseudo? Serious or not? An inquiry into psychopathological and clinical features of a common phenomenon. Psychopathology 35 (2002), 296–302.
48. 48 van Os, J., Linscott, R.J., Myin-Germeys, I., Delespaul, P., Krabbendam, L., A systematic review and meta-analysis of the psychosis continuum: Evidence for a psychosis proneness-persistence-impairment model of psychotic disorder. Psychol Med 39 (2009), 179–195.
49. 49 Galdos, M., Simons, C., Fernandez-Rivas, A., Wichers, M., Peralta, C., Lataster, T., et al. Affectively salient meaning in random noise: a task sensitive to psychosis liability. Schizophr Bull 37 (2011), 1179–1186.
50. 50 Diederen, K.M., van Lutterveld, R., Sommer, I.E., Neuroimaging of voice hearing in non-psychotic individuals: A mini review. Front Hum Neurosci, 6, 2012, 111.
51. 51 Laroi, F., Sommer, I.E., Blom, J.D., Fernyhough, C., Ffytche, D.H., Hugdahl, K., et al. The characteristic features of auditory verbal hallucinations in clinical and nonclinical groups: State-of-the-art overview and future directions. Schizophr Bull 38 (2012), 724–733.
52. 52 Johns, L.C., Kompus, K., Connell, M., Humpston, C., Lincoln, T.M., Longden, E., et al. Auditory verbal hallucinations in persons with and without a need for care. Schizophr Bull 40:Suppl 4 (2014), S255–S264.
53. 53 de Leede-Smith, S., Barkus, E., A comprehensive review of auditory verbal hallucinations: Lifetime prevalence, correlates and mechanisms in healthy and clinical individuals. Front Hum Neurosci, 7, 2013, 367.
54. 54 Johns, L.C., Nazroo, J.Y., Bebbington, P., Kuipers, E., Occurrence of hallucinatory experiences in a community sample and ethnic variations. Br J Psychiatry 180 (2002), 174–178.
55. 55 Teufel, C., Subramaniam, N., Dobler, V., Perez, J., Finnemann, J., Mehta, P.R., et al. Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals. Proc Natl Acad Sci U S A., 2015.
56. 56 Ellson, D.G., Hallucinations produced by sensory conditioning. J Exp Psychol, 1941, 1.
57. 57 Kot, T., Serper, M., Increased susceptibility to auditory conditioning in hallucinating schizophrenic patients: A preliminary investigation. J Nerv Ment Dis 190 (2002), 282–288.
58. 58 Warburton, D.M., Wesnes, K., Edwards, J., Larrad, D., Scopolamine and the sensory conditioning of hallucinations. Neuropsychobiology 14 (1985), 198–202.
59. 59 Agathon, M., Roussel, A., [Use of a sensory conditioning test in patients treated with psychotropic drugs]. Int Pharmacopsychiatry 8 (1973), 221–233.
60. 60 Brogden, W.J., Sensory pre-conditioning of human subjects. J Exp Psychol 37 (1947), 527–539.
61. 61 Whitson, J.A., Galinsky, A.D., Lacking control increases illusory pattern perception. Science 322 (2008), 115–117.
62. 62 Sutton, R., Proceedings of the 7th Yale Workshop on Adaptive and Learning Systems. 1992, Yale University Press, New Haven, Connecticut, 161–166.
63. 63 Anderson, B.D.O., Moore, J.B., Optimal Filtering. 1979, Prentice-Hall, Englewood Cliffs, New Jersey.
64. 64 Dayan, P., Kakade, S., Montague, P.R., Learning and selective attention. Nat Neurosci 3:Suppl (2000), 1218–1223.
65. 65 Iglesias, S., Mathys, C., Brodersen, K.H., Kasper, L., Piccirelli, M., den Ouden, H.E., et al. Hierarchical prediction errors in midbrain and basal forebrain during sensory learning. Neuron 80 (2013), 519–530.
66. 66 Park, H.J., Friston, K., Structural and functional brain networks: From connections to cognition. Science, 342, 2013, 1238411.
67. 67 Allen, M., Fardo, F., Dietz, M.J., Hillebrandt, H., Friston, K.J., Rees, G., et al. Anterior insula coordinates hierarchical processing of tactile mismatch responses. NeuroImage 127 (2015), 34–43.
68. 68 Shergill, S.S., Brammer, M.J., Amaro, E., Williams, S.C., Murray, R.M., McGuire, P.K., Temporal course of auditory hallucinations. Br J Psychiatry 185 (2004), 516–517.
69. 69 Sommer, I.E., Diederen, K.M., Blom, J.D., Willems, A., Kushan, L., Slotema, K., et al. Auditory verbal hallucinations predominantly activate the right inferior frontal area. Brain 131 (2008), 3169–3177.
70. 70 Geddes, M.R., Tie, Y., Gabrieli, J.D., McGinnis, S.M., Golby, A.J., Whitfield-Gabrieli, S., Altered functional connectivity in lesional peduncular hallucinosis with REM sleep behavior disorder. Cortex 74 (2016), 96–106.
71. 71 Hurley, L.M., Devilbiss, D.M., Waterhouse, B.D., A matter of focus: Monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr Opin Neurobiol 14 (2004), 488–495.
72. 72 Yu, A.J., Dayan, P., Uncertainty, neuromodulation, and attention. Neuron 46 (2005), 681–692.
73. 73 Servan-Schreiber, D., Printz, H., Cohen, J.D., A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. Science 249 (1990), 892–895.
74. 74 Eldar, E., Cohen, J.D., Niv, Y., The effects of neural gain on attention and learning. Nat Neurosci 16 (2013), 1146–1153.
75. 75 Summerfield, C., Koechlin, E., A neural representation of prior information during perceptual inference. Neuron 59 (2008), 336–347.
76. 76 Blanke, O., Landis, T., Seeck, M., Electrical cortical stimulation of the human prefrontal cortex evokes complex visual hallucinations. Epilepsy Behav 1 (2000), 356–361.
77. 77 Mc, L.T., Meyer, A., Anatomical correlates of improvement after leucotomy. J Ment Sci 95 (1949), 182–196.
78. 78 Gratton, C., Nomura, E.M., Perez, F., D'Esposito, M., Focal brain lesions to critical locations cause widespread disruption of the modular organization of the brain. J Cogn Neurosci 24 (2012), 1275–1285.
79. 79 van den Heuvel, M.P., Sporns, O., Rich-club organization of the human connectome. J Neurosci 31 (2011), 15775–15786.
80. 80 Whitfield-Gabrieli, S., Thermenos, H.W., Milanovic, S., Tsuang, M.T., Faraone, S.V., McCarley, R.W., et al. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci U S A 106 (2009), 1279–1284.
81. 81 Carhart-Harris, R.L., Friston, K.J., The default-mode, ego-functions and free-energy: A neurobiological account of Freudian ideas. Brain 133 (2010), 1265–1283.
82. 82 van den Heuvel, M.P., Sporns, O., Collin, G., Scheewe, T., Mandl, R.C., Cahn, W., et al. Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70 (2013), 783–792.
83. 83 Chanes, L., Barrett, L.F., Redefining the role of limbic areas in cortical processing. Trends Cogn Sci 20 (2016), 96–106.
84. 84 Dehaene, S., Kerszberg, M., Changeux, J.P., A neuronal model of a global workspace in effortful cognitive tasks. Proc Natl Acad Sci U S A 95 (1998), 14529–14534.
85. 85 Dehaene, S., Changeux, J.P., Experimental and theoretical approaches to conscious processing. Neuron 70 (2011), 200–227.
86. 86 Fodor, J., The Modularity of Mind: An Essay on Faculty Psychology. 1983, MIT Press, Cambridge, Massachusetts: Harvard.
87. 87 Friston, K.J., Price, C.J., Modules and brain mapping. Cogn Neuropsychol 28 (2011), 241–250.
88. 88 Colombo, M., Colombo, M., Moving forward (and beyond) the modularity debate: A network perspective. Philosophy Sci, 80, 2013, 3.
89. 89 Penny, W.D., Stephan, K.E., Mechelli, A., Friston, K.J., Comparing dynamic causal models. NeuroImage 22 (2004), 1157–1172.
90. 90 Curcic-Blake, B., Liemburg, E., Vercammen, A., Swart, M., Knegtering, H., Bruggeman, R., et al. When Broca goes uninformed: reduced information flow to Broca's area in schizophrenia patients with auditory hallucinations. Schizophr Bull 39 (2013), 1087–1095.
91. 91 Barrett, L.F., Simmons, W.K., Interoceptive predictions in the brain. Nat Rev Neurosci 16 (2015), 419–429.
92. 92 van den Heuvel, M.P., Sporns, O., An anatomical substrate for integration among functional networks in human cortex. J Neurosci 33 (2013), 14489–14500.
93. 93 Hohwy, J., Roepstorff, A., Friston, K., Predictive coding explains binocular rivalry: An epistemological review. Cognition 108 (2008), 687–701.
94. 94 Einhauser, W., Stout, J., Koch, C., Carter, O., Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc Natl Acad Sci U S A 105 (2008), 1704–1709.
95. 95 Hoffman, R.E., Quinlan, D.M., Mazure, C.M., McGlashan, T.M., Cortical instability and the mechanism of mania: A neural network simulation and perceptual test. Biologic Psychiatry 49 (2001), 500–509.
96. 96 McBain, R., Norton, D.J., Kim, J., Chen, Y., Reduced cognitive control of a visually bistable image in schizophrenia. J Int Neuropsychologic Soc 17 (2011), 551–556.
97. 97 Tononi, G., Edelman, G.M., Schizophrenia and the mechanisms of conscious integration. Brain Res Brain Res Rev 31 (2000), 391–400.
98. 98 Tononi, G., Sporns, O., Edelman, G.M., A measure for brain complexity: Relating functional segregation and integration in the nervous system. Proc Natl Acad Sci U S A 91 (1994), 5033–5037.
99. 99 Lupyan, G., Clark, A., Words and the world: Predictive coding and the language-perception-cognition interface. Curr Direct Psychol Sci 24 (2015), 279–284.
100. 100 Dakin, S., Carlin, P., Hemsley, D., Weak suppression of visual context in chronic schizophrenia. Curr Biol 15 (2005), R822–R824.
101. 101 Koethe, D., Gerth, C.W., Neatby, M.A., Haensel, A., Thies, M., Schneider, U., et al. Disturbances of visual information processing in early states of psychosis and experimental delta-9-tetrahydrocannabinol altered states of consciousness. Schizophr Res 88 (2006), 142–150.
102. 102 Teufel, C., Subramaniam, N., Dobler, V., Perez, J., Finnemann, J., Mehta, P.R., et al. Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals. Proc Natl Acad Sci U S A 112 (2015), 13401–13406.
103. 103 Norton, D., Ongur, D., Stromeyer, C. 3rd, Chen, Y., Altered ‘three-flash’ illusion in response to two light pulses in schizophrenia. Schizophr Res 103 (2008), 275–282.
104. 104 Ford, J.M., Studying auditory verbal hallucinations using the RDoC framework. Psychophysiology 53 (2016), 298–304.
105. 105 Adams, R.A., Stephan, K.E., Brown, H.R., Frith, C.D., Friston, K.J., The computational anatomy of psychosis. Front Psychiatry, 4, 2013, 47.
106. 106 Powers, A.R. III, Gancsos, M.G., Finn, E.S., Morgan, P.T., Corlett, P.R., Ketamine-induced hallucinations. Psychopathology 48 (2015), 376–385.
107. 107 Corlett, P.R., Frith, C.D., Fletcher, P.C., From drugs to deprivation: A Bayesian framework for understanding models of psychosis. Psychopharmacology 206 (2009), 515–530.
108. 108 Horga, G., Schatz, K.C., Abi-Dargham, A., Peterson, B.S., Deficits in predictive coding underlie hallucinations in schizophrenia. J Neurosci 34 (2014), 8072–8082.
109. 109 Notredame, C.E., Pins, D., Deneve, S., Jardri, R., What visual illusions teach us about schizophrenia. Front Integr Neurosci, 8, 2014, 63.
110. 110 Arieti, S., An overview of schizophrenia from a predominantly psychological approach. Am J Psychiatry 131 (1974), 241–249.
111. 111 Hoffman, R.E., Revisiting Arieti's “listening attitude” and hallucinated voices. Schizophr Bull 36 (2010), 440–442.
112. 112 Jardri, R., Deneve, S., Circular inferences in schizophrenia. Brain 136 (2013), 3227–3241.
113. 113 Collerton, D., Perry, E., McKeith, I., Why people see things that are not there: A novel perception and attention deficit model for recurrent complex visual hallucinations. Behav Brain Sci 28 (2005), 737–757.
114. 114 Phillips, W.A., Clark, A., Silverstein, S.M., On the functions, mechanisms, and malfunctions of intracortical contextual modulation. Neurosci Biobehav Rev 52 (2015), 1–20.
115. 115 Corlett, P.R., Fletcher, P.C., Computational psychiatry: A Rosetta Stone linking the brain to mental illness. Lancet Psychiatry, 2014.
116. 116 Sass, L.A., Paradoxes of Delusion: Wittgenstein, Schreber, and the Schizophrenic Mind. 1994, Cornell University Press, Ithaca, New York.
117. 117 Mikles, N.L., Laycock, J.P., Tracking the tulpa. Nova Religio: J Altern Emergent Religions 19 (2015), 87–97.
118. 118 Cichy, R.M., Heinzle, J., Haynes, J.D., Imagery and perception share cortical representations of content and location. Cereb Cortex 22 (2012), 372–380.
119. 119 Ffytche, D.H., Visual hallucinations and the Charles Bonnet syndrome. Curr Psychiatry Rep 7 (2005), 168–179.
120. 120 Seth, A.K., Suzuki, K., Critchley, H.D., An interoceptive predictive coding model of conscious presence. Front Psychol, 2, 2011, 395.
121. 121 Manita, S., Suzuki, T., Homma, C., Matsumoto, T., Odagawa, M., Yamada, K., et al. A top-down cortical circuit for accurate sensory perception. Neuron 86 (2015), 1304–1316.
122. 122 Seth, A.K., A predictive processing theory of sensorimotor contingencies: Explaining the puzzle of perceptual presence and its absence in synesthesia. Cogn Neurosci 5 (2014), 97–118.
123. 123 van Leeuwen, T.M., Singer, W., Nikolic, D., The merit of synesthesia for consciousness research. Front Psychol, 6, 2015, 1850.