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.
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References
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
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
Alho K (1995) Cerebral generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound changes. Ear Hear 16(1): 38–51
Anderson LA, Christianson GB, Linden JF (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29(22): 7359–7363
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
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
Barry RJ (2009) Habituation of the orienting reflex and the development of Preliminary Process Theory. Neurobiol Learn Memory 92(2): 235–242
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
Boehnke SE, Munoz DP (2008) On the importance of the transient visual response in the superior colliculus. Curr Opin Neurobiol 18(6): 544–551
Bradley MM (2009) Natural selective attention: orienting and emotion. Psychophysiology 46(1): 1–11
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
Brosch M, Schreiner CE (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77(2): 923–943
Calford MB, Semple MN (1995) Monaural inhibition in cat auditory cortex. J Neurophysiol 73(5): 1876–1891
Dong S, Clayton DF (2009) Habituation in songbirds. Neurobiol Learn Mem 92(2): 183–188
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
Eytan D, Brenner N, Marom S (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23(28): 9349–9356
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
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
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
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
Gaither NS, Stein BE (1979) Reptiles and mammals use similar sensory organizations in the midbrain. Science 205(4406): 595–597
Glanzman DL (2009) Habituation in Aplysia: the Cheshire cat of neurobiology. Neurobiol Learn Memory 92(2): 147–154
Gottlieb JP, Kusunoki M, Goldberg ME (1998) The representation of visual salience in monkey parietal cortex. Nature 391(6666): 481–484
Gutfreund Y, Knudsen EI (2006) Adaptation in the auditory space map of the barn owl. J Neurophysiol 17: 17
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
Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284(5417): 1158–1161
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
Ingham NJ, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91(2): 632–645
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
Kane NM, Curry SH, Butler SR, Cummins BH (1993) Electrophysiological indicator of awakening from coma. Lancet 341(8846): 688
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
Katz Y, Heiss JE, Lampl I (2006) Cross-whisker adaptation of neurons in the rat barrel cortex. J Neurosci 26(51): 13363–13372
Kayser C, Petkov CI, Lippert M, Logothetis NK (2005) Mechanisms for allocating auditory attention: an auditory saliency map. Curr Biol 15(21): 1943–1947
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
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
Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2(9): 1177–1194
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
Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 6: 6
Knudsen EI (2011) Control from below: the role of a midbrain network in spatial attention. Eur J Neurosci 33(11): 1961–1972
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
Knudsen EI, Konishi M (1978) A neural map of auditory space in the owl. Science 200(4343): 795–797
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
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
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
Lovejoy LP, Krauzlis RJ (2009) Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat Neurosci 13(2): 261–266
Luksch H (2003) Cytoarchitecture of the avian optic tectum: neuronal substrate for cellular computation. Rev Neurosci 14(1–2): 85–106
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
Marom S (2009) Neural timescales or lack thereof. Prog Neurobiol 90(1): 16–28
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
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
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
McPeek RM, Keller EL (2002) Saccade target selection in the superior colliculus during a visual search task. J Neurophysiol 88(4): 2019–2034
Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42: 135–159
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
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
Moiseff A (1989) Bi-coordinate sound localization by the barn owl. J Comp Physiol A 164(5): 637–644
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
Muller JR, Metha AB, Krauskopf J, Lennie P (1999) Rapid adaptation in visual cortex to the structure of images. Science 285(5432): 1405–1408
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
Mysore SP, Knudsen EI (2011) The role of a midbrain network in competitive stimulus selection. Curr Opin Neurobiol 21(4): 653–660
Mysore SP, Asadollahi A, Knudsen EI (2010) Global inhibition and stimulus competition in the owl optic tectum. J Neurosci 30(5): 1727–1738
Mysore SP, Asadollahi A, Knudsen EI (2011) Signaling of the strongest stimulus in the owl optic tectum. J Neurosci 31(14): 5186–5196
Naatanen R (1995) The mismatch negativity: a powerful tool for cognitive neuroscience. Ear Hear 16(1): 6–18
Naatanen R, Tervaniemi M, Sussman E, Paavilainen P, Winkler I (2001) “Primitive intelligence” in the auditory cortex. Trends Neurosci 24(5): 283–288
Nelken I (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Curr Opin Neurobiol 14(4): 474–480
Nelken I, Ulanovsky N (2007) Mismatch negativity and stimulus- specific adaptation in animal models. J Psychophysiol 21(3–4): 214–223
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
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
Perez-Gonzalez D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22(11): 2879–2885
Pluta SR, Rowland BA, Stanford TR, Stein BE (2011) Alterations to multisensory and unisensory integration by stimulus competition. J Neurophysiol 106(6): 3091–3101
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
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
Posner MI (1980) Orienting of attention. Q J Exp Psychol 32(1): 3–25
Posner MI (1981) Cognition and neural systems. Cognition 10(1–3): 261–266
Reches A, Gutfreund Y (2008) Stimulus-specific adaptations in the gaze control system of the barn owl. J Neurosci 28(6): 1523–1533
Reches A, Gutfreund Y (2009) Auditory and multisensory responses in the tectofugal pathway of the barn owl. J Neurosci 29(30): 9602–9613
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
Robinson DL, Petersen SE (1992) The pulvinar and visual salience. Trends Neurosci 15(4): 127–132
Rodgers CK, Munoz DP, Scott SH, Pare M (2006) Discharge properties of monkey tectoreticular neurons. J Neurophysiol 95(6): 3502–3511
Sams M, Paavilainen P, Alho K, Naatanen R (1985) Auditory frequency discrimination and event-related potentials. Electroencephalogr Clin Neurophysiol 62(6): 437–448
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
Sokolov EN (1963) Higher nervous functions; the orienting reflex. Annu Rev Physiol 25: 545–580
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
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
Stein BE, Meredith MA (1993) The Merging of the senses. Cognitive neuroscience series. MIT Press, Cambridge
Taaseh N, Yaron A, Nelken I (2011) Stimulus-specific adaptation and deviance detection in the rat auditory cortex. PLoS One 6(8): e23369
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
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
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
Thompson RF (2009) Habituation: a history. Neurobiol Learn Memory 92(2): 127–134
Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73(1): 16–43
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
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
Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6(4): 391–398
Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24(46): 10440–10453
Valentinuzzi VS, Ferrari EA (1997) Habituation to sound during morning and night sessions in pigeons (Columba livia). Physiol Behav 62(6): 1203–1209
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
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
Wehr M, Zador AM (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47(3): 437–445
Weinberger NM, Oleson TD, Ashe JH (1975) Sensory system neural activity during habituation of the pupillary orienting reflex. Behav Biol 15(3): 283–301
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
Winkler I, Denham SL, Nelken I (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cogn Sci 13(12): 532–540
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
Winkowski DE, Knudsen EI (2007) Top-down control of multimodal sensitivity in the barn owl optic tectum. J Neurosci 27(48): 13279–13291
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
Woods EJ, Frost BJ (1977) Adaptation and habituation characteristics of tectal neurons in the pigeon. Exp Brain Res 27(3–4): 347–354
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
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
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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DOI: https://doi.org/10.1007/s00422-012-0497-3