Saliency mapping in the optic tectum and its relationship to habituation

Frontiers in Integrative Neuroscience

Volumn 8, Issue JAN, 2014, Pages

  Dutta, Arkadeb ^a   Gutfreund, Yoram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Barn owl; Habituation; Optic tectum; Orienting response; Saliency map; Spatial attention; Superior colliculus

Indexed keywords

ANIMAL BEHAVIOR; ATTENTION; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN MAPPING; EVOLUTIONARY ADAPTATION; EVOLUTIONARY HOMOLOGY; GAZE; HABITUATION; MEMORY; MISMATCH NEGATIVITY; NERVE POTENTIAL; NONHUMAN; ORIENTING RESPONSE; OWL; PRIMATE; PROBABILITY; REVIEW; SALIENCY MAPPING; SENSORIMOTOR INTEGRATION; STATE DEPENDENT LEARNING; STIMULUS SPECIFIC ADAPTATION; SUPERIOR COLLICULUS; SYNAPTIC INHIBITION; VISUAL STIMULATION;

EID: 84892602832     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2014.00001     Document Type: Review

References (127)

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, 3647-3668.
2. Albeck, Y., and Konishi, M. (1995). Responses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals. J. Neurophysiol. 74, 1689-1700.
3. Anderson, B. A. (2013). A value-driven mechanism of attentional selection. J. Vis. 13, 7. doi: 10.1167/13.3.7
4. Anderson, L. A., Christianson, G. B., and Linden, J. F. (2009). Stimulus-specific adaptation occurs in the auditory thalamus. J. Neurosci. 29, 7359-7363. doi: 10.1523/JNEUROSCI.0793-09.2009
5. Antunes, F. M., Nelken, I., Covey, E., and Malmierca, M. S. (2010). Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS ONE 5:e14071. doi: 10.1371/journal.pone.0014071
6. Ayala, Y. A., Perez-Gonzalez, D., Duque, D., Nelken, I., and Malmierca, M.S. (2013). Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus. Front. Neural Circuits 6:119. doi: 10.3389/fncir.2012.00119
7. Ayala, Y. A., and Malmierca, M. S. (2013). Stimulus-specific adaptation and deviance detection in the inferior colliculus. Front. Neural Circuits 6:89. doi: 10.3389/fncir.2012.00089
8. Bala, A. D., and Takahashi, T. T. (2000). Pupillary dilation response as an indicator of auditory discrimination in the barn owl. J. Comp. Physiol. A 186, 425-434. doi: 10.1007/s003590050442
9. Barry, R. J. (2009). Habituation of the orienting reflex and the development of Preliminary Process Theory. Neurobiol. Learn. Mem. 92, 235-242. doi: 10.1016/j.nlm.2008.07.007
10. Basso, M. A., Powers, A. S., and Evinger, C. (1996). An explanation for reflex blink hyperexcitability in Parkinson's disease. I. Superior colliculus. J. Neurosci. 16, 7308-7317.
11. Bischof, H. J., and Watanabe, S. (1997). On the structure and function of the tectofugal visual pathway in laterally eyed birds. Eur. J. Morphol. 35, 246-254. doi: 10.1076/ejom.35.4.246.13080
12. Boehnke, S. E., Berg, D. J., Marino, R. A., Baldi, P. F., Itti, L., and Munoz, D. P. (2011). Visual adaptation and novelty responses in the superior colliculus. Eur. J. Neurosci. 34, 766-779. doi: 10.1111/j.1460-9568.2011.07805.x
13. Boehnke, S. E., and Munoz, D. P. (2008). On the importance of the transient visual response in the superior colliculus. Curr. Opin. Neurobiol. 18, 544-551. doi: 10.1016/j.conb.2008.11.004
14. Booth, J. R., Burman, D. D., Meyer, J. R., Lei, Z., Trommer, B. L., Davenport, N. D., et al. (2005). Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). J. Child Psychol. Psychiatry 46, 94-111. doi: 10.1111/j.1469-7610.2004. 00337.x
15. Bradley, M. M. (2009). Natural selective attention: orienting and emotion. Psychophysiology 46, 1-11. doi: 10.1111/j.1469-8986.2008.00702.x
16. Brosch, M., and Schreiner, C. E. (1997). Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77, 923-943.
17. Butler, A. B., and Hodos, W. (2005). Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. Hoboken, NJ: John Wiley & Sons. doi: 10.1002/0471733849
18. Calford, M. B., and Semple, M. N. (1995). Monaural inhibition in cat auditory cortex. J. Neurophysiol. 73, 1876-1891.
19. Corneil, B. D., Munoz, D. P., and Olivier, E. (2007). Priming of head premotor circuits during oculomotor preparation. J. Neurophysiol. 97, 701-714. doi: 10.1152/jn.00670.2006
20. Dean, P., Redgrave, P., and Westby, G. W. (1989). Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12, 137-147. doi: 10.1016/0166-2236(89)90052-0
21. Dong, S., and Clayton, D. F. (2009). Habituation in songbirds. Neurobiol. Learn. Mem. 92, 183-188. doi: 10.1016/j.nlm.2008.09.009
22. Dukewich, K. R. (2009). Reconceptualizing inhibition of return as habituation of the orienting response. Psychon. Bull. Rev. 16, 238-251. doi: 10.3758/PBR.16.2.238
23. Euston, D. R., and Takahashi, T. T. (2002). From spectrum to space: the contribution of level difference cues to spatial receptive fields in the barn owl inferior colliculus. J. Neurosci. 22, 284-293.
24. Eytan, D., Brenner, N., and Marom, S. (2003). Selective adaptation in networks of cortical neurons. J. Neurosci. 23, 9349-9356.
25. Farley, B. J., Quirk, M. C., Doherty, J. J., and Christian, E. P. (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, 16475-16484. doi: 10.1523/JNEUROSCI.2793-10.2010
26. Fecteau, J. H., and Munoz, D. P. (2005). Correlates of capture of attention and inhibition of return across stages of visual processing. J. Cogn. Neurosci. 17, 1714-1727. doi: 10.1162/089892905774589235
27. Fecteau, J. H., and Munoz, D. P. (2006). Salience, relevance, and firing: a priority map for target selection. Trends Cogn. Sci. 10, 382-390. doi: 10.1016/j.tics.2006.06.011
28. Fishman, Y. I., and Steinschneider, M. (2012). Searching for the mismatch negativity in primary auditory cortex of the awake monkey: deviance detection or stimulus specific adaptation? J. Neurosci. 32, 15747-15758. doi: 10.1523/JNEUROSCI.2835-12.2012
29. Furukawa, S., Maki, K., Kashino, M., and 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, 3313-3326. doi: 10.1152/jn.01219.2004
30. Gaither, N. S., and Stein, B. E. (1979). Reptiles and mammals use similar sensory organizations in the midbrain. Science 205, 595-597. doi: 10.1126/science.451623
31. Gitelman, D. R. (2003). Attention and its disorders. Br. Med. Bull. 65, 21-34. doi: 10.1093/bmb/65.1.21
32. Glanzman, D. L. (2009). Habituation in Aplysia: the Cheshire cat of neurobiology. Neurobiol. Learn. Mem. 92, 147-154. doi: 10.1016/j.nlm.2009.03.005
33. Gnadt, J. W., Lu, S. M., Breznen, B., Basso, M. A., Henriquez, V. M., and Evinger, C. (1997). Influence of the superior colliculus on the primate blink reflex. Exp. Brain Res. 116, 389-398. doi: 10.1007/PL00005767
34. Gottlieb, J. P., Kusunoki, M., and Goldberg, M. E. (1998). The representation of visual salience in monkey parietal cortex. Nature 391, 481-484. doi: 10.1038/35135
35. Gutfreund, Y. (2012). Stimulus-specific adaptation, habituation and change detection in the gaze control system. Biol. Cybern. 106, 657-668. doi: 10.1007/s00422-012-0497-3
36. Gutfreund, Y., and Knudsen, E. I. (2006). Adaptation in the auditory space map of the barn owl. J. Neurophysiol. 96, 813-825. doi: 10.1152/jn.01144.2005
37. Herrero, L., Rodriguez, F., Salas, C., and Torres, B. (1998). Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp. Brain Res. 120, 291-305. doi: 10.1007/s002210050403
38. Horwitz, G.D., and Newsome, W.T. (1999). Separate signals for target selection and movement specification in the superior colliculus. Science 284, 1158-1161. doi: 10.1126/science.284.5417.1158
39. Horwitz, G. D., and Newsome, W. T. (2001). Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task. J. Neurophysiol. 86, 2543-2558.
40. Ingham, N. J., and McAlpine, D. (2004). Spike-frequency adaptation in the inferior colliculus. J. Neurophysiol. 91, 632-645. doi: 10.1152/jn.00779.2003
41. Ingle, D. (1975). Focal attention in the frog: behavioral and physiological correlates. Science 188, 1033-1035. doi: 10.1126/science.1170636
42. Itti, L., and Koch, C. (2000). A saliency-based search mechanism for overt and covert shifts of visual attention. Vision Res. 40, 1489-1506. doi: 10.1016/S0042-6989(99)00163-7
43. Itti, L., and Koch, C. (2001). Computational modelling of visual attention. Nat. Rev. Neurosci. 2, 194-203. doi: 10.1038/35058500
44. Katz, Y., Heiss, J. E., and Lampl, I. (2006). Cross-whisker adaptation of neurons in the rat barrel cortex. J. Neurosci. 26, 13363-13372. doi: 10.1523/JNEUROSCI.4056-06.2006
45. Keay, K. A., Redgrave, P., and Dean, P. (1988). Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus. Brain Res. Bull. 20, 13-26. doi: 10.1016/0361-9230(88)90004-4
46. King, A. J. (2004). The superior colliculus. Curr. Biol. 14, R335-R338. doi: 10.1016/j.cub.2004.04.018
47. King, A.J., and Palmer, A.R. (1985). Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp. Brain Res. 60, 492-500. doi: 10.1007/BF00236934
48. Knudsen, E. I. (1982). Auditory and visual maps of space in the optic tectum of the owl. J. Neurosci. 2, 1177-1194.
49. Knudsen, E. I. (2007). Fundamental Components of Attention. Annu. Rev. Neurosci. 6, 6.
50. Knudsen, E. I. (2011). Control from below: the role of a midbrain network in spatial attention. Eur. J. Neurosci. 33, 1961-1972. doi: 10.1111/j.1460-9568.2011.07696.x
51. Krauzlis, R. J., Lovejoy, L. P., and Zenon, A. (2013). Superior colliculus and visual spatial attention. Annu. Rev. Neurosci. 36, 165-182. doi: 10.1146/annurev-neuro-062012-170249
52. Lai, D., Brandt, S., Luksch, H., and Wessel, R. (2011). Recurrent antitopographic inhibition mediates competitive stimulus selection in an attention network. J. Neurophysiol. 105, 793-805. doi: 10.1152/jn.00673.2010
53. Lovejoy, L. P., and Krauzlis, R. J. (2009). Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat. Neurosci. 13, 261-266. doi: 10.1038/nn.2470
54. Luksch, H. (2003). Cytoarchitecture of the avian optic tectum: neuronal substrate for cellular computation. Rev. Neurosci. 14, 85-106. doi: 10.1515/REVNEURO.2003.14.1-2.85
55. Malmierca, M. S., Cristaudo, S., Perez-Gonzalez, D., and Covey, E. (2009). Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J. Neurosci. 29, 5483-5493. doi: 10.1523/JNEUROSCI.4153-08.2009
56. Marin, G. J., Duran, E., Morales, C., Gonzalez-Cabrera, C., Sentis, E., Mpodozis, J., et al. (2012). Attentional capture? Synchronized feedback signals from the isthmi boost retinal signals to higher visual areas. J. Neurosci. 32, 1110-1122. doi: 10.1523/JNEUROSCI.4151-11.2012
57. Marin, G., Mpodozis, J., Sentis, E., Ossandon, T., and Letelier, J. C. (2005). Oscillatory bursts in the optic tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis. J. Neurosci. 25, 7081-7089. doi: 10.1523/JNEUROSCI.1379-05.2005
58. Marin, G., Salas, C., Sentis, E., Rojas, X., Letelier, J. C., and Mpodozis, J. (2007). A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J. Neurosci. 27, 8112-8121. doi: 10.1523/JNEUROSCI.1420-07.2007
59. Marom, S. (2009). Neural timescales or lack thereof. Prog. Neurobiol. 90, 16-28. doi: 10.1016/j.pneurobio.2009.10.003
60. Maximino, C. (2008). Evolutionary changes in the complexity of the tectum of nontetrapods: a cladistic approach. PLoS ONE 3:e3582. doi: 10.1371/journal.pone.0003582
61. McAlpine, D., Jiang, D., Shackleton, T.M., and Palmer, A.R. (2000). Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. J. Neurophysiol. 83, 1356-1365.
62. McHaffie, J. G., and Stein, B. E. (1982). Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res. 247, 243-253. doi: 10.1016/0006-8993(82)91249-5
63. McPeek, R. M., and Keller, E. L. (2002). Saccade target selection in the superior colliculus during a visual search task. J. Neurophysiol. 88, 2019-2034.
64. McPeek, R. M., and Keller, E. L. (2004). Deficits in saccade target selection after inactivation of superior colliculus. Nat. Neurosci. 7, 757-763. doi: 10.1038/nn1269
65. Meredith, M. A., Nemitz, J. W., and Stein, B. E. (1987). Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors. J. Neurosci. 7, 3215-3229.
66. Meredith, M. A., and Stein, B. E. (1986). Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J. Neurophysiol. 56, 640-662.
67. Mize, R. R., and Murphy, E. H. (1976). Alterations in receptive field properties of superior colliculus cells produced by visual cortex ablation in infant and adult cats. J. Comp. Neurol. 168, 393-424. doi: 10.1002/cne.901680306
68. Moiseff, A., and Konishi, M. (1981). Neuronal and behavioral sensitivity to binaural time differences in the owl. J. Neurosci. 1, 40-48.
69. Muller, J. R., Metha, A. B., Krauskopf, J., and Lennie, P. (1999). Rapid adaptation in visual cortex to the structure of images. Science 285, 1405-1408. doi: 10.1126/science.285.5432.1405
70. Mysore, S. P., Asadollahi, A., and Knudsen, E. I. (2010). Global inhibition and stimulus competition in the owl optic tectum. J. Neurosci. 30, 1727-1738. doi: 10.1523/JNEUROSCI.3740-09.2010
71. Mysore, S. P., Asadollahi, A., and Knudsen, E. I. (2011). Signaling of the strongest stimulus in the owl optic tectum. J. Neurosci. 31, 5186-5196. doi: 10.1523/JNEUROSCI.4592-10.2011
72. Mysore, S. P., and Knudsen, E. I. (2011a). Flexible categorization of relative stimulus strength by the optic tectum. J. Neurosci. 31, 7745-7752. doi: 10.1523/JNEUROSCI.5425-10.2011
73. Mysore, S. P., and Knudsen, E. I. (2011b). The role of a midbrain network in competitive stimulus selection. Curr. Opin. Neurobiol 21, 653-660. doi: 10.1016/j.conb.2011.05.024
74. Mysore, S. P., and Knudsen, E. I. (2013). A shared inhibitory circuit for both exogenous and endogenous control of stimulus selection. Nat. Neurosci. 16, 473-478.
75. Naatanen, R. (1995). The mismatch negativity: a powerful tool for cognitive neuroscience. Ear Hear. 16, 6-18.
76. Nelken, I. (2004). Processing of complex stimuli and natural scenes in the auditory cortex. Curr. Opin. Neurobiol. 14, 474-480. doi: 10.1016/j.conb.2004.06.005
77. Nelken, I., and Ulanovsky, N. (2007). Mismatch negativity and stimulus-specific adaptation in animal models. J. Psychophysiol. 21, 214-223. doi: 10.1027/0269-8803.21.34.214
78. Nelken, I., Yaron, A., Polterovich, A., and Hershenhoren, I. (2013). Stimulus-specific adaptation beyond pure tones. Adv. Exp. Med. Biol. 787, 411-418. doi: 10.1007/978-1-4614-1590-9_45
79. Netser, S., Ohayon, S., and Gutfreund, Y. (2010). Multiple manifestations of micros-timulation in the optic tectum: eye movements, pupil dilations, and sensory priming. J. Neurophysiol. 104, 108-118. doi: 10.1152/jn.01142.2009
80. Netser, S., Zahar, Y., and Gutfreund, Y. (2011). Stimulus-specific adaptation: can it be a neural correlate of behavioral habituation? J. Neurosci. 31, 17811-17820. doi: 10.1523/JNEUROSCI.4790-11.2011574
81. Nodal, F. R., Doubell, T. P., Jiang, Z. D., Thompson, I. D., and King, A. J. (2005). Development of the projection from the nucleus of the brachium of the inferior colliculus to the superior colliculus in the ferret. J. Comp. Neurol. 485, 202-217. doi: 10.1002/cne.20478
82. Oleson, T.D., Westenberg, I.S., and Weinberger, N. M. (1972). Characteristics of the pupillary dilation response during Pavlovian conditioning in paralyzed cats. Behav. Biol. 7, 829-840. doi: 10.1016/S0091-6773(72)80175-5
83. Perez-Gonzalez, D., Malmierca, M. S., and Covey, E. (2005). Novelty detector neurons in the mammalian auditory midbrain. Eur. J. Neurosci. 22, 2879-2885. doi: 10.1111/j.1460-9568.2005.04472.x
84. Pluta, S. R., Rowland, B. A., Stanford, T. R., and Stein, B. E. (2011). Alterations to multisensory and unisensory integration by stimulus competition. J. Neurophysiol. 106, 3091-3101. doi: 10.1152/jn.00509.2011
85. Posner, M. I. (1980). Orienting of attention. Q. J. Exp. Psychol. 32, 3-25. doi: 10.1080/00335558008248231
86. Reches, A., and Gutfreund, Y. (2008). Stimulus-specific adaptations in the gaze control system of the barn owl. J. Neurosci. 28, 1523-1533. doi: 10.1523/JNEUROSCI.3785-07.2008
87. Reches, A., and Gutfreund, Y. (2009). Auditory and multisensory responses in the tectofugal pathway of the barn owl. J. Neurosci. 29, 9602-9613. doi: 10.1523/JNEUROSCI.6117-08.2009
88. Reches, A., Netser, S., and Gutfreund, Y. (2010). Interactions between stimulus-specific adaptation and visual auditory integration in the forebrain of the barn owl. J. Neurosci. 30, 6991-6998. doi: 10.1523/JNEUROSCI.5723-09. 2010
89. Redgrave, P., and Dean, P. (1985). Tonic desynchronisation of cortical electroencephalogram by electrical and chemical stimulation of superior colliculus and surrounding structures in urethane-anaesthetised rats. Neuroscience 16, 659-671. doi: 10.1016/0306-4522(85)90199-X
90. Richardson, B. D., Hancock, K. E., and Caspary, D. M. (2013). Stimulus-specific adaptation in auditory thalamus of young and aged awake rats. J Neurophysiol. 110, 1892-902. doi: 10.1152/jn.00403.2013
91. Robinson, D. L., and Petersen, S. E. (1992). The pulvinar and visual salience. Trends Neurosci. 15, 127-132. doi: 10.1016/0166-2236(92)90354-B
92. Sawa, M., and Ohtsuka, K. (1994). Lens accommodation evoked by microstimulation of the superior colliculus in the cat. Vision Res. 34, 975-981. doi: 10.1016/0042-6989(94)90001-9
93. Shimizu, T., and Karten, H. J. (1993). The avian visual system and the evolution of the neocortex, in Vision, Brain, and Behavior in Birds, eds H. P. Zeigler and H. J. Bischof (Cambridge: MIT press), 103-114.
94. Siddle, D. A. (1991). Orienting, habituation, and resource allocation: an associative analysis. Psychophysiology 28, 245-259. doi: 10.1111/j.1469-8986.1991.tb02190.x
95. Sokolov, E. N. (1963). Higher nervous functions; the orienting reflex. Annu. Rev. Physiol. 25, 545-580. doi: 10.1146/annurev.ph.25.030163.002553
96. Sparks, D. L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol. Rev. 66, 118-171.
97. Spitzer, M. W., Bala, A. D., and Takahashi, T. T. (2003). Auditory spatial discrimination by barn owls in simulated echoic conditions. J. Acoust. Soc. Am. 113, 1631-1645. doi: 10.1121/1.1548152
98. Stanford, T. R., Quessy, S., and Stein, B. E. (2005). Evaluating the operations underlying multisensory integration in the cat superior colliculus. J. Neurosci. 25, 6499-6508. doi: 10.1523/JNEUROSCI.5095-04.2005
99. Stein, B. E., and Meredith, M. A. (1993). The Merging of the Senses. Cambridge: MIT Press.
100. Stelmack, R. M., and Siddle, D. A. (1982). Pupillary dilation as an index of the orienting reflex. Psychophysiology 19, 706-708. doi: 10.1111/j.1469-8986.1982.tb02529.x
101. Taaseh, N., Yaron, A., and Nelken, I. (2011). Stimulus-specific adaptation and deviance detection in the rat auditory cortex. PLoS ONE 6:e23369. doi: 10.1371/journal.pone.0023369
102. Takada, M., Itoh, K., Yasui, Y., Sugimoto, T., and 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, 385-396. doi: 10.1007/BF00235934
103. Takahashi, T., Moiseff, A., and Konishi, M. (1984). Time and intensity cues are processed independently in the auditory system of the owl. J. Neurosci. 4, 1781-1786.
104. Takahashi, T. T., and Konishi, M. (1988). Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl. J. Comp. Neurol. 274, 190-211. doi: 10.1002/cne.902740206
105. Thompson, R. F. (2009). Habituation: a history. Neurobiol. Learn. Mem. 92, 127-134. doi: 10.1016/j.nlm.2008.07.011
106. Thompson, R. F., Patterson, M. M., and Teyler, T. J. (1972). The neurophysiology of learning. Annu. Rev. Psychol. 23, 73-104. doi: 10.1146/annurev.ps.23.020172.000445
107. Thompson, R. F., and Spencer, W. A. (1966). Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16-43. doi: 10.1037/h0022681
108. Tiitinen, H., May, P., Reinikainen, K., and Naatanen, R. (1994). Attentive novelty detection in humans is governed by pre-attentive sensory memory. Nature 372, 90-92. doi: 10.1038/372090a0
109. Tsodyks, M. V., and Markram, H. (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl. Acad. Sci. U.S.A. 94, 719-723. doi: 10.1073/pnas.94.2.719
110. Ulanovsky, N., Las, L., Farkas, D., and Nelken, I. (2004). Multiple time scales of adaptation in auditory cortex neurons. J. Neurosci. 24, 10440-10453. doi: 10.1523/JNEUROSCI.1905-04.2004
111. Ulanovsky, N., Las, L., and Nelken, I. (2003). Processing of low-probability sounds by cortical neurons. Nat. Neurosci. 6, 391-398. doi: 10.1038/nn1032
112. Valentinuzzi, V. S., and Ferrari, E. A. (1997). Habituation to sound during morning and night sessions in pigeons (Columba livia). Physiol. Behav. 62, 1203-1209. doi: 10.1016/S0031-9384(97)00009-7
113. Varela, J. A., Sen, K., Gibson, J., Fost, J., Abbott, L. F., and Nelson, S. B. (1997). A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J. Neurosci. 17, 7926-7940.
114. von der Behrens, W., Bauerle, P., Kossl, M., and Gaese, B. H. (2009). Correlating stimulus-specific adaptation of cortical neurons and local field potentials in the awake rat. J. Neurosci. 29, 13837-13849. doi: 10.1523/JNEUROSCI.3475-09.2009
115. Wallace, M. T., Wilkinson, L. K., and Stein, B. E. (1996). Representation and integration of multiple sensory inputs in primate superior colliculus. J. Neurophysiol. 76, 1246-1266.
116. Wang, C. A., Boehnke, S. E., White, B. J., and Munoz, D. P. (2012). Micros-timulation of the monkey superior colliculus induces pupil dilation without evoking saccades. J. Neurosci. 32, 3629-3636. doi: 10.1523/JNEUROSCI.5512-11. 2012
117. Wang, Y., Luksch, H., Brecha, N. C., and Karten, H. J. (2006). Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): a possible substrate for synchronizing tectal channels. J. Comp. Neurol. 494, 7-35. doi: 10.1002/cne.20821
118. Wehr, M., and Zador, A. M. (2005). Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47, 437-445. doi: 10.1016/j.neuron.2005.06.009
119. Weinberger, N. M., Oleson, T. D., and Ashe, J. H. (1975). Sensory system neural activity during habituation of the pupillary orienting reflex. Behav. Biol. 15, 283-301. doi: 10.1016/S0091-6773(75)91695-8
120. Weisbard, C., and Graham, P. K. (1971). Heart-rate change as a component of the orienting response in monkeys. J. Comp. Physiol. Psychol. 76, 74-83. doi: 10.1037/h0031048
121. Westerman, L. A., and Smith, R. L. (1984). Rapid and short-term adaptation in auditory nerve responses. Hear. Res. 15, 249-260. doi: 10.1016/0378-5955(84)90032-7
122. Winkler, I., Denham, S. L., and Nelken, I. (2009). Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cogn. Sci. 13, 532-540. doi: 10.1016/j.tics.2009.09.003
123. Winkowski, D. E., and Knudsen, E. I. (2006). Top-down gain control of the auditory space map by gaze control circuitry in the barn owl. Nature 439, 336-339. doi: 10.1038/nature04411
124. Winkowski, D. E., and Knudsen, E. I. (2007). Top-down control of multimodal sensitivity in the barn owl optic tectum. J. Neurosci. 27, 13279-13291. doi: 10.1523/JNEUROSCI.3937-07.2007
125. Woods, E. J., and Frost, B. J. (1977). Adaptation and habituation characteristics of tectal neurons in the pigeon. Exp. Brain Res. 27, 347-354.
126. Zahar, Y., Reches, A., and Gutfreund, Y. (2009). Multisensory enhancement in the optic tectum of the barn owl: spike count and spike timing. J Neurophysiol. 101, 2380-2394. doi: 10.1152/jn.91193.2008
127. 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, 44-58. doi: 10.1016/j.ijpsycho.2005.05.003