Stimulus-specific adaptation, habituation and change detection in the gaze control system

Abstract

This prospect article addresses the neurobiology of detecting and responding to changes or unexpected events. Change detection is an ongoing computational task performed by the brain as part of the broader process of saliency mapping and selection of the next target for attention. In the optic tectum (OT) of the barn owl, the probability of the stimulus has a dramatic influence on the neural response to that stimulus; rare or deviant stimuli induce stronger responses compared to common stimuli. This phenomenon, known as stimulus-specific adaptation, has recently attracted scientific interest because of its possible role in change detection. In the barn owl’s OT, it may underlie the ability to orient specifically to unexpected events and is therefore opening new directions for research on the neurobiology of fundamental psychological phenomena such as habituation, attention, and surprise.

References

  1. Adolphs R (1993) Bilateral inhibition generates neuronal responses tuned to interaural level differences in the auditory brainstem of the barn owl. J Neurosci 13(9): 3647–3668

    CAS  PubMed  Google Scholar 

  2. Albeck Y, Konishi M (1995) Responses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals. J Neurophysiol 74(4): 1689–1700

    CAS  PubMed  Google Scholar 

  3. Alho K (1995) Cerebral generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound changes. Ear Hear 16(1): 38–51

    CAS  PubMed  Google Scholar 

  4. Anderson LA, Christianson GB, Linden JF (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29(22): 7359–7363

    CAS  PubMed  Google Scholar 

  5. Antunes FM, Nelken I, Covey E, Malmierca MS (2010) Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS One 5(11): e14071

    PubMed Central  PubMed  Google Scholar 

  6. Bala AD, Takahashi TT (2000) Pupillary dilation response as an indicator of auditory discrimination in the barn owl. J Comp Physiol [A] 186(5): 425–434

    CAS  Google Scholar 

  7. Barry RJ (2009) Habituation of the orienting reflex and the development of Preliminary Process Theory. Neurobiol Learn Memory 92(2): 235–242

    Google Scholar 

  8. Bischof HJ, Watanabe S (1997) On the structure and function of the tectofugal visual pathway in laterally eyed birds. Eur J Morphol 35(4): 246–254

    CAS  PubMed  Google Scholar 

  9. Boehnke SE, Munoz DP (2008) On the importance of the transient visual response in the superior colliculus. Curr Opin Neurobiol 18(6): 544–551

    CAS  PubMed  Google Scholar 

  10. Bradley MM (2009) Natural selective attention: orienting and emotion. Psychophysiology 46(1): 1–11

    PubMed Central  PubMed  Google Scholar 

  11. Brainard MS, Knudsen EI (1998) Sensitive periods for visual calibration of the auditory space map in the barn owl optic tectum. J Neurosci 18(10): 3929–3942

    CAS  PubMed  Google Scholar 

  12. Brosch M, Schreiner CE (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77(2): 923–943

    CAS  PubMed  Google Scholar 

  13. Calford MB, Semple MN (1995) Monaural inhibition in cat auditory cortex. J Neurophysiol 73(5): 1876–1891

    CAS  PubMed  Google Scholar 

  14. Dong S, Clayton DF (2009) Habituation in songbirds. Neurobiol Learn Mem 92(2): 183–188

    PubMed Central  PubMed  Google Scholar 

  15. Euston DR, Takahashi TT (2002) From spectrum to space: the contribution of level difference cues to spatial receptive fields in the barn owl inferior colliculus. J Neurosci 22(1): 284–293

    CAS  PubMed  Google Scholar 

  16. Eytan D, Brenner N, Marom S (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23(28): 9349–9356

    CAS  PubMed  Google Scholar 

  17. Farley BJ, Quirk MC, Doherty JJ, Christian EP (2010) Stimulus-specific adaptation in auditory cortex is an NMDA-independent process distinct from the sensory novelty encoded by the mismatch negativity. J Neurosci 30(49): 16475–16484

    CAS  PubMed  Google Scholar 

  18. Fecteau JH, Munoz DP (2005) Correlates of capture of attention and inhibition of return across stages of visual processing. J Cogn Neurosci 17(11): 1714–1727

    PubMed  Google Scholar 

  19. Feldman DE, Knudsen EI (1997) An anatomical basis for visual calibration of the auditory space map in the barn owl’s midbrain. J Neurosci 17(17): 6820–6837

    CAS  PubMed  Google Scholar 

  20. Furukawa S, Maki K, Kashino M, Riquimaroux H (2005) Dependency of the interaural phase difference sensitivities of inferior collicular neurons on a preceding tone and its implications in neural population coding. J Neurophysiol 93(6): 3313–3326

    PubMed  Google Scholar 

  21. Gaither NS, Stein BE (1979) Reptiles and mammals use similar sensory organizations in the midbrain. Science 205(4406): 595–597

    CAS  PubMed  Google Scholar 

  22. Glanzman DL (2009) Habituation in Aplysia: the Cheshire cat of neurobiology. Neurobiol Learn Memory 92(2): 147–154

    CAS  Google Scholar 

  23. Gottlieb JP, Kusunoki M, Goldberg ME (1998) The representation of visual salience in monkey parietal cortex. Nature 391(6666): 481–484

    CAS  PubMed  Google Scholar 

  24. Gutfreund Y, Knudsen EI (2006) Adaptation in the auditory space map of the barn owl. J Neurophysiol 17: 17

    Google Scholar 

  25. Herrero L, Rodriguez F, Salas C, Torres B (1998) Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120(3): 291–305

    CAS  PubMed  Google Scholar 

  26. Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284(5417): 1158–1161

    CAS  PubMed  Google Scholar 

  27. Hyde PS, Knudsen EI (2000) Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl [In Process Citation]. J Comp Neurol 421(2): 146–160

    CAS  PubMed  Google Scholar 

  28. Ingham NJ, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91(2): 632–645

    PubMed  Google Scholar 

  29. Itti L, Koch C (2000) A saliency-based search mechanism for overt and covert shifts of visual attention. Vision Res 40(10–12): 1489–1506

    CAS  PubMed  Google Scholar 

  30. Kane NM, Curry SH, Butler SR, Cummins BH (1993) Electrophysiological indicator of awakening from coma. Lancet 341(8846): 688

    CAS  PubMed  Google Scholar 

  31. Karten HJ, Hodos W, Nauta WJ, Revzin AM (1973) Neural connections of the “visual wulst” of the avian telencephalon. Experimental studies in the piegon (Columba livia) and owl (Speotyto cunicularia). J Comp Neurol 150(3): 253–278

    CAS  PubMed  Google Scholar 

  32. Katz Y, Heiss JE, Lampl I (2006) Cross-whisker adaptation of neurons in the rat barrel cortex. J Neurosci 26(51): 13363–13372

    CAS  PubMed  Google Scholar 

  33. Kayser C, Petkov CI, Lippert M, Logothetis NK (2005) Mechanisms for allocating auditory attention: an auditory saliency map. Curr Biol 15(21): 1943–1947

    CAS  PubMed  Google Scholar 

  34. King AJ, Hutchings ME (1987) Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space. J Neurophysiol 57(2): 596–624

    CAS  PubMed  Google Scholar 

  35. King AJ, Palmer AR (1985) Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp Brain Res 60(3): 492–500

    CAS  PubMed  Google Scholar 

  36. Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2(9): 1177–1194

    CAS  PubMed  Google Scholar 

  37. Knudsen EI (1987) Neural derivation of sound source location in the barn owl. An example of a computational map. Ann N Y Acad Sci 510: 33–38

    CAS  PubMed  Google Scholar 

  38. Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 6: 6

    Google Scholar 

  39. Knudsen EI (2011) Control from below: the role of a midbrain network in spatial attention. Eur J Neurosci 33(11): 1961–1972

    PubMed Central  PubMed  Google Scholar 

  40. Knudsen EI, Knudsen PF (1983) Space-mapped auditory projections from the inferior colliculus to the optic tectum in the barn owl (Tyto alba). J Comp Neurol 218(2): 187–196

    CAS  PubMed  Google Scholar 

  41. Knudsen EI, Konishi M (1978) A neural map of auditory space in the owl. Science 200(4343): 795–797

    CAS  PubMed  Google Scholar 

  42. Knudsen EI, Cohen YE, Masino T (1995) Characterization of a forebrain gaze field in the archistriatum of the barn owl: microstimulation and anatomical connections. J Neurosci 15(7 Pt 2): 5139–5151

    CAS  PubMed  Google Scholar 

  43. Lai D, Brandt S, Luksch H, Wessel R (2011) Recurrent antitopographic inhibition mediates competitive stimulus selection in an attention network. J Neurophysiol 105(2): 793–805

    PubMed Central  PubMed  Google Scholar 

  44. Lewald J, Dorrscheidt GJ (1998) Spatial-tuning properties of auditory neurons in the optic tectum of the pigeon. Brain Res 790(1–2): 339–342

    CAS  PubMed  Google Scholar 

  45. Lovejoy LP, Krauzlis RJ (2009) Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat Neurosci 13(2): 261–266

    PubMed Central  PubMed  Google Scholar 

  46. Luksch H (2003) Cytoarchitecture of the avian optic tectum: neuronal substrate for cellular computation. Rev Neurosci 14(1–2): 85–106

    PubMed  Google Scholar 

  47. Malmierca MS, Cristaudo S, Perez-Gonzalez D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29(17): 5483–5493

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Marom S (2009) Neural timescales or lack thereof. Prog Neurobiol 90(1): 16–28

    PubMed  Google Scholar 

  49. Masino T, Knudsen EI (1992) Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl. Exp Brain Res 92(2): 194–208

    CAS  PubMed  Google Scholar 

  50. McAlpine D, Jiang D, Shackleton TM, Palmer AR (2000) Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. J Neurophysiol 83(3): 1356–1365

    CAS  PubMed  Google Scholar 

  51. McHaffie JG, Stein BE (1982) Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247(2): 243–253

    CAS  PubMed  Google Scholar 

  52. McPeek RM, Keller EL (2002) Saccade target selection in the superior colliculus during a visual search task. J Neurophysiol 88(4): 2019–2034

    PubMed  Google Scholar 

  53. Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42: 135–159

    CAS  PubMed  Google Scholar 

  54. Mill R, Coath M, Wennekers T, Denham SL (2011) A neurocomputational model of stimulus-specific adaptation to oddball and Markov sequences. PLoS Comput Biol 7(8): e1002117

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Mize RR, Murphy EH (1976) Alterations in receptive field properties of superior colliculus cells produced by visual cortex ablation in infant and adult cats. J Comp Neurol 168(3): 393–424

    CAS  PubMed  Google Scholar 

  56. Moiseff A (1989) Bi-coordinate sound localization by the barn owl. J Comp Physiol A 164(5): 637–644

    CAS  PubMed  Google Scholar 

  57. Moiseff A, Konishi M (1983) Binaural characteristics of units in the owl’s brainstem auditory pathway: precursors of restricted spatial receptive fields. J Neurosci 3(12): 2553–2562

    CAS  PubMed  Google Scholar 

  58. Muller JR, Metha AB, Krauskopf J, Lennie P (1999) Rapid adaptation in visual cortex to the structure of images. Science 285(5432): 1405–1408

    CAS  PubMed  Google Scholar 

  59. Muller JR, Philiastides MG, Newsome WT (2005) Microstimulation of the superior colliculus focuses attention without moving the eyes. Proc Natl Acad Sci USA 102(3): 524–529

    PubMed Central  PubMed  Google Scholar 

  60. Mysore SP, Knudsen EI (2011) The role of a midbrain network in competitive stimulus selection. Curr Opin Neurobiol 21(4): 653–660

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Mysore SP, Asadollahi A, Knudsen EI (2010) Global inhibition and stimulus competition in the owl optic tectum. J Neurosci 30(5): 1727–1738

    CAS  PubMed Central  PubMed  Google Scholar 

  62. Mysore SP, Asadollahi A, Knudsen EI (2011) Signaling of the strongest stimulus in the owl optic tectum. J Neurosci 31(14): 5186–5196

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Naatanen R (1995) The mismatch negativity: a powerful tool for cognitive neuroscience. Ear Hear 16(1): 6–18

    CAS  PubMed  Google Scholar 

  64. Naatanen R, Tervaniemi M, Sussman E, Paavilainen P, Winkler I (2001) “Primitive intelligence” in the auditory cortex. Trends Neurosci 24(5): 283–288

    CAS  PubMed  Google Scholar 

  65. Nelken I (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Curr Opin Neurobiol 14(4): 474–480

    CAS  PubMed  Google Scholar 

  66. Nelken I, Ulanovsky N (2007) Mismatch negativity and stimulus- specific adaptation in animal models. J Psychophysiol 21(3–4): 214–223

    Google Scholar 

  67. Netser S, Ohayon S, Gutfreund Y (2010) Multiple manifestations of microstimulation in the optic tectum: eye movements, pupil dilations, and sensory priming. J Neurophysiol 104(1): 108–118

    PubMed  Google Scholar 

  68. Netser S, Zahar Y, Gutfreund Y (2011) Stimulus specific adaptation: can it be a neural correlate of behavioral habituation?. J Neurosci 31(49): 17811–17820

    CAS  PubMed  Google Scholar 

  69. Perez-Gonzalez D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22(11): 2879–2885

    PubMed  Google Scholar 

  70. Pluta SR, Rowland BA, Stanford TR, Stein BE (2011) Alterations to multisensory and unisensory integration by stimulus competition. J Neurophysiol 106(6): 3091–3101

    PubMed Central  PubMed  Google Scholar 

  71. Poganiatz I, Wagner H (2001) Sound-localization experiments with barn owls in virtual space: influence of broadband interaural level different on head-turning behavior. J Comp Physiol [A] 187(3): 225–233

    CAS  Google Scholar 

  72. Poganiatz I, Nelken I, Wagner H (2001) Sound-localization experiments with barn owls in virtual space: influence of interaural time difference on head-turning behavior. J Assoc Res Otolaryngol 2(1): 1–21

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Posner MI (1980) Orienting of attention. Q J Exp Psychol 32(1): 3–25

    CAS  PubMed  Google Scholar 

  74. Posner MI (1981) Cognition and neural systems. Cognition 10(1–3): 261–266

    CAS  PubMed  Google Scholar 

  75. Reches A, Gutfreund Y (2008) Stimulus-specific adaptations in the gaze control system of the barn owl. J Neurosci 28(6): 1523–1533

    CAS  PubMed  Google Scholar 

  76. Reches A, Gutfreund Y (2009) Auditory and multisensory responses in the tectofugal pathway of the barn owl. J Neurosci 29(30): 9602–9613

    CAS  PubMed  Google Scholar 

  77. Reches A, Netser S, Gutfreund Y (2010) Interactions between stimulus-specific adaptation and visual auditory integration in the forebrain of the barn owl. J Neurosci 30(20): 6991–6998

    CAS  PubMed  Google Scholar 

  78. Robinson DL, Petersen SE (1992) The pulvinar and visual salience. Trends Neurosci 15(4): 127–132

    CAS  PubMed  Google Scholar 

  79. Rodgers CK, Munoz DP, Scott SH, Pare M (2006) Discharge properties of monkey tectoreticular neurons. J Neurophysiol 95(6): 3502–3511

    PubMed  Google Scholar 

  80. Sams M, Paavilainen P, Alho K, Naatanen R (1985) Auditory frequency discrimination and event-related potentials. Electroencephalogr Clin Neurophysiol 62(6): 437–448

    CAS  PubMed  Google Scholar 

  81. Shimizu T, Karten HJ (1993) The avian visual system and the evolution of the neocortex. In: Zeigler HP, Bischof HJ (eds) Vision, brain, and behavior in birds. MIT, Cambridge, pp 103–114

    Google Scholar 

  82. Sokolov EN (1963) Higher nervous functions; the orienting reflex. Annu Rev Physiol 25: 545–580

    CAS  PubMed  Google Scholar 

  83. Sparks DL (1986) Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol Rev 66(1): 118–171

    CAS  PubMed  Google Scholar 

  84. Spitzer MW, Bala AD, Takahashi TT (2003) Auditory spatial discrimination by barn owls in simulated echoic conditions. J Acoust Soc Am 113(3): 1631–1645

    PubMed  Google Scholar 

  85. Stein BE, Meredith MA (1993) The Merging of the senses. Cognitive neuroscience series. MIT Press, Cambridge

    Google Scholar 

  86. Taaseh N, Yaron A, Nelken I (2011) Stimulus-specific adaptation and deviance detection in the rat auditory cortex. PLoS One 6(8): e23369

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Takada M, Itoh K, Yasui Y, Sugimoto T, Mizuno N (1985) Topographical projections from the posterior thalamic regions to the striatum in the cat, with reference to possible tecto-thalamo-striatal connections. Exp Brain Res 60(2): 385–396

    CAS  PubMed  Google Scholar 

  88. Takahashi TT, Konishi M (1988) Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl. J Comp Neurol 274(2): 190–211

    CAS  PubMed  Google Scholar 

  89. Takahashi T, Moiseff A, Konishi M (1984) Time and intensity cues are processed independently in the auditory system of the owl. J Neurosci 4(7): 1781–1786

    CAS  PubMed  Google Scholar 

  90. Thompson RF (2009) Habituation: a history. Neurobiol Learn Memory 92(2): 127–134

    Google Scholar 

  91. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73(1): 16–43

    CAS  PubMed  Google Scholar 

  92. Tiitinen H, May P, Reinikainen K, Naatanen R (1994) Attentive novelty detection in humans is governed by pre-attentive sensory memory. Nature 372(6501): 90–92

    CAS  PubMed  Google Scholar 

  93. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94(2): 719–723

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6(4): 391–398

    CAS  PubMed  Google Scholar 

  95. Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24(46): 10440–10453

    CAS  PubMed  Google Scholar 

  96. Valentinuzzi VS, Ferrari EA (1997) Habituation to sound during morning and night sessions in pigeons (Columba livia). Physiol Behav 62(6): 1203–1209

    CAS  PubMed  Google Scholar 

  97. Varela JA, Sen K, Gibson J, Fost J, Abbott LF, Nelson SB (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17(20): 7926–7940

    CAS  PubMed  Google Scholar 

  98. von der Behrens W, Bauerle P, Kossl M, Gaese BH (2009) Correlating stimulus-specific adaptation of cortical neurons and local field potentials in the awake rat. J Neurosci 29(44): 13837–13849

    PubMed  Google Scholar 

  99. Wehr M, Zador AM (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47(3): 437–445

    CAS  PubMed  Google Scholar 

  100. Weinberger NM, Oleson TD, Ashe JH (1975) Sensory system neural activity during habituation of the pupillary orienting reflex. Behav Biol 15(3): 283–301

    CAS  PubMed  Google Scholar 

  101. Weisbard C, Graham PK (1971) Heart-rate change as a component of the orienting response in monkeys. J Comp Physiol Psychol 76(1): 74–83

    CAS  PubMed  Google Scholar 

  102. Winkler I, Denham SL, Nelken I (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cogn Sci 13(12): 532–540

    PubMed  Google Scholar 

  103. Winkowski DE, Knudsen EI (2006) Top-down gain control of the auditory space map by gaze control circuitry in the barn owl. Nature 439(7074): 336–339

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Winkowski DE, Knudsen EI (2007) Top-down control of multimodal sensitivity in the barn owl optic tectum. J Neurosci 27(48): 13279–13291

    CAS  PubMed Central  PubMed  Google Scholar 

  105. Winkowski DE, Knudsen EI (2008) Distinct mechanisms for top-down control of neural gain and sensitivity in the owl optic tectum. Neuron 60(4): 698–708

    CAS  PubMed Central  PubMed  Google Scholar 

  106. Woods EJ, Frost BJ (1977) Adaptation and habituation characteristics of tectal neurons in the pigeon. Exp Brain Res 27(3–4): 347–354

    CAS  PubMed  Google Scholar 

  107. Zahar Y, Reches A, Gutfreund Y (2009) Multisensory enhancement in the optic tectum of the barn owl: spike count and spike timing. J Neurophysiol 101(5): 2380–2394

    PubMed  Google Scholar 

  108. Zimmer H (2006) Habituation of the orienting response as reflected by the skin conductance response and by endogenous event-related brain potentials. Int J Psychophysiol 60(1): 44–58

    PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the Israel Science Foundation and the Institute for Psychobiology in Israel. The author thanks Amit Reches, Yael Zahar, and Shai Netser.

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Gutfreund, Y. Stimulus-specific adaptation, habituation and change detection in the gaze control system. Biol Cybern 106, 657–668 (2012). https://doi.org/10.1007/s00422-012-0497-3

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Keywords

  • Optic tectum
  • Barn owl
  • Novely detection
  • Auditory
  • Superior colliculus
  • Adaptation
  • Orienting response