1932

Abstract

Coordination between different sensory systems is a necessary element of sensory processing. Where and how signals from different sense organs converge onto common neural circuitry have become topics of increasing interest in recent years. In this article, we focus specifically on visual–auditory interactions in areas of the mammalian brain that are commonly considered to be auditory in function. The auditory cortex and inferior colliculus are two key points of entry where visual signals reach the auditory pathway, and both contain visual- and/or eye movement–related signals in humans and other animals. The visual signals observed in these auditory structures reflect a mixture of visual modulation of auditory-evoked activity and visually driven responses that are selective for stimulus location or features. These key response attributes also appear in the classic visual pathway but may play a different role in the auditory pathway: to modify auditory rather than visual perception. Finally, while this review focuses on two particular areas of the auditory pathway where this question has been studied, robust descending as well as ascending connections within this pathway suggest that undiscovered visual signals may be present at other stages as well.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-091517-034003
2021-09-15
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/vision/7/1/annurev-vision-091517-034003.html?itemId=/content/journals/10.1146/annurev-vision-091517-034003&mimeType=html&fmt=ahah

Literature Cited

  1. Adams JC. 1980. Crossed and descending projections to the inferior colliculus. Neurosci. Lett. 19:1–5
    [Google Scholar]
  2. Angelucci A, Clasca F, Sur M. 1998. Brainstem inputs to the ferret medial geniculate nucleus and the effect of early deafferentation on novel retinal projections to the auditory thalamus. J. Comp. Neurol. 400:417–39
    [Google Scholar]
  3. Ashida G, Carr CE. 2011. Sound localization: Jeffress and beyond. Curr. Opin. Neurobiol. 21:745–51
    [Google Scholar]
  4. Atilgan H, Town SM, Wood KC, Jones GP, Maddox RK et al. 2018. Integration of visual information in auditory cortex promotes auditory scene analysis through multisensory binding. Neuron 97:640–55.e4
    [Google Scholar]
  5. Bala AD, Takahashi TT. 2000. Pupillary dilation response as an indicator of auditory discrimination in the barn owl. J. Comp. Physiol. A 186:425–34
    [Google Scholar]
  6. Bedny M, Pascual-Leone A, Dodell-Feder D, Fedorenko E, Saxe R 2011. Language processing in the occipital cortex of congenitally blind adults. PNAS 108:4429–34
    [Google Scholar]
  7. Bergan JF, Knudsen EI. 2009. Visual modulation of auditory responses in the owl inferior colliculus. J. Neurophysiol. 101:2924–33
    [Google Scholar]
  8. Bernstein LE, Auer ET Jr., Moore JK, Ponton CW, Don M, Singh M. 2002. Visual speech perception without primary auditory cortex activation. Neuroreport 13:311–15
    [Google Scholar]
  9. Bizley JK, King AJ. 2008. Visual-auditory spatial processing in auditory cortical neurons. Brain Res 1242:24–36
    [Google Scholar]
  10. Bizley JK, Nodal FR, Bajo VM, Nelken I, King AJ. 2007. Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb. Cortex 17:2172–89
    [Google Scholar]
  11. Bola Ł, Zimmermann M, Mostowski P, Jednoróg K, Marchewka A et al. 2017. Task-specific reorganization of the auditory cortex in deaf humans. PNAS 114:E600–9
    [Google Scholar]
  12. Boynton GM, Engel SA, Glover GH, Heeger DJ. 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 16:4207–21
    [Google Scholar]
  13. Brainard MS, Knudsen EI. 1993a. Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl. J. Neurosci. 13:4589–608
    [Google Scholar]
  14. Brainard MS, Knudsen EI. 1993b. Visual calibration of the neural representation of auditory space in the barn owl. Biomed. Res. 14:35–40
    [Google Scholar]
  15. Brosch M, Selezneva E, Scheich H. 2005. Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys. J. Neurosci. 25:6797–806
    [Google Scholar]
  16. Brosch M, Selezneva E, Scheich H. 2015. Neuronal activity in primate auditory cortex during the performance of audiovisual tasks. Eur. J. Neurosci. 41:603–14
    [Google Scholar]
  17. Budinger E, Scheich H. 2009. Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex. Hear. Res. 258:16–27
    [Google Scholar]
  18. Bulkin DA, Groh JM. 2011. Systematic mapping of the monkey inferior colliculus reveals enhanced low frequency sound representation. J. Neurophysiol. 105:1785–97
    [Google Scholar]
  19. Bulkin DA, Groh JM. 2012a. Distribution of eye position information in the monkey inferior colliculus. J. Neurophysiol. 107:785–95
    [Google Scholar]
  20. Bulkin DA, Groh JM. 2012b. Distribution of visual and saccade related information in the monkey inferior colliculus. Front. Neural Circuits 6:61
    [Google Scholar]
  21. Calvert GA, Brammer MJ, Bullmore ET, Campbell R, Iversen SD, David AS. 1999. Response amplification in sensory-specific cortices during crossmodal binding. Neuroreport 10:2619–23
    [Google Scholar]
  22. Calvert GA, Bullmore ET, Brammer MJ, Campbell R, Williams SC et al. 1997. Activation of auditory cortex during silent lipreading. Science 276:593–96
    [Google Scholar]
  23. Cao Y, Summerfield C, Park H, Giordano BL, Kayser C. 2019. Causal inference in the multisensory brain. Neuron 102:1076–87.e8
    [Google Scholar]
  24. Chandrasekaran C, Lemus L, Ghazanfar AA 2013. Dynamic faces speed up the onset of auditory cortical spiking responses during vocal detection. PNAS 110:E4668–77
    [Google Scholar]
  25. Chandrasekaran C, Trubanova A, Stillittano S, Caplier A, Ghazanfar AA. 2009. The natural statistics of audiovisual speech. PLOS Comput. Biol. 5:e1000436
    [Google Scholar]
  26. Coleman JR, Clerici WJ. 1987. Sources of projections to subdivisions of the inferior colliculus in the rat. J. Comp. Neurol. 262:215–26
    [Google Scholar]
  27. Cooper MH, Young PA. 1976. Cortical projections to the inferior colliculus of the cat. Exp. Neurol. 51:488–502
    [Google Scholar]
  28. da Costa NM, Martin KA, Sägesser FD. 2018. A weighted graph of the projections to mouse auditory cortex. bioRxiv 228726. https://doi.org/10.1101/228726
    [Crossref]
  29. DeBello WM, Feldman DE, Knudsen EI. 2001. Adaptive axonal remodeling in the midbrain auditory space map. J. Neurosci. 21:3161–74
    [Google Scholar]
  30. Doubell TP, Baron J, Skaliora I, King AJ. 2000. Topographical projection from the superior colliculus to the nucleus of the brachium of the inferior colliculus in the ferret: convergence of visual and auditory information. Eur. J. Neurosci. 12:4290–308
    [Google Scholar]
  31. du Lac S, Knudsen EI 1991. Early visual deprivation results in a degraded motor map in the optic tectum of barn owls. PNAS 88:3426–30
    [Google Scholar]
  32. Falchier A, Clavagnier S, Barone P, Kennedy H. 2002. Anatomical evidence of multimodal integration in primate striate cortex. J. Neurosci. 22:5749–59
    [Google Scholar]
  33. Falchier A, Schroeder CE, Hackett TA, Lakatos P, Nascimento-Silva S et al. 2010. Projection from visual areas V2 and prostriata to caudal auditory cortex in the monkey. Cereb. Cortex 20:1529–38
    [Google Scholar]
  34. Feldman DE, Brainard MS, Knudsen EI. 1996. Newly learned auditory responses mediated by NMDA receptors in the owl inferior colliculus. Science 271:525–28
    [Google Scholar]
  35. Feldman DE, Knudsen EI. 1997. An anatomical basis for visual calibration of the auditory space map in the barn owl's midbrain. J. Neurosci. 17:6820–37
    [Google Scholar]
  36. Feldman DE, Knudsen EI. 1998a. Experience-dependent plasticity and the maturation of glutamatergic synapses. Neuron 20:1067–71
    [Google Scholar]
  37. Feldman DE, Knudsen EI. 1998b. Pharmacological specialization of learned auditory responses in the inferior colliculus of the barn owl. J. Neurosci. 18:3073–87
    [Google Scholar]
  38. Finney EM, Fine I, Dobkins KR. 2001. Visual stimuli activate auditory cortex in the deaf. Nat. Neurosci. 4:1171–73
    [Google Scholar]
  39. Fishman MC, Michael P. 1973. Integration of auditory information in the cat's visual cortex. Vis. Res. 13:1415–19
    [Google Scholar]
  40. Gastinger MJ, O'Brien JJ, Larsen NB, Marshak DW. 1999. Histamine immunoreactive axons in the macaque retina. Investig. Ophthalmol. Vis. Sci. 40:487–95
    [Google Scholar]
  41. Gau R, Bazin PL, Trampel R, Turner R, Noppeney U 2020. Resolving multisensory and attentional influences across cortical depth in sensory cortices. eLife 9:e46856
    [Google Scholar]
  42. Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK. 2005. Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J. Neurosci. 25:5004–12
    [Google Scholar]
  43. Groh JM. 2014a. Making Space: How the Brain Knows Where Things Are Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  44. Groh JM. 2014b. Moving with maps and meters. See Groh 2014a 143–59
  45. Groh JM, Kelly KA, Underhill AM. 2003. A monotonic code for sound azimuth in primate inferior colliculus. J. Cogn. Neurosci. 15:1217–31
    [Google Scholar]
  46. Groh JM, Sparks DL. 1992. Two models for transforming auditory signals from head-centered to eye-centered coordinates. Biol. Cybern. 67:291–302
    [Google Scholar]
  47. Groh JM, Trause AS, Underhill AM, Clark KR, Inati S. 2001. Eye position influences auditory responses in primate inferior colliculus. Neuron 29:509–18
    [Google Scholar]
  48. Gruters KG, Groh JM. 2012. Sounds and beyond: multisensory and other non-auditory signals in the inferior colliculus. Front. Neural Circuits 6:96
    [Google Scholar]
  49. Gruters KG, Murphy DLK, Jenson CD, Smith DW, Shera CA, Groh JM 2018. The eardrums move when the eyes move: a multisensory effect on the mechanics of hearing. PNAS 115:E1309–18
    [Google Scholar]
  50. Gutfreund Y, Zheng W, Knudsen EI. 2002. Gated visual input to the central auditory system. Science 297:1556–59
    [Google Scholar]
  51. Hall AJ, Lomber SG. 2008. Auditory cortex projections target the peripheral field representation of primary visual cortex. Exp. Brain Res. 190:413–30
    [Google Scholar]
  52. Harting JK. 1977. Descending pathways from the superior collicullus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J. Comp. Neurol. 173:583–612
    [Google Scholar]
  53. Hartline PH, Vimal RL, King AJ, Kurylo DD, Northmore DP. 1995. Effects of eye position on auditory localization and neural representation of space in superior colliculus of cats. Exp. Brain Res. 104:402–8
    [Google Scholar]
  54. Hoffman KL, Ghazanfar AA, Gauthier I, Logothetis NK. 2007. Category-specific responses to faces and objects in primate auditory cortex. Front. Syst. Neurosci. 1:2
    [Google Scholar]
  55. Huffman RF, Henson OW. 1990. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res. Rev. 15:295–323
    [Google Scholar]
  56. Itaya SK, Van Hoesen GW. 1982. Retinal innervation of the inferior colliculus in rat and monkey. Brain Res 233:45–52
    [Google Scholar]
  57. Jack CE, Thurlow WR. 1973. Effects of degree of visual association and angle of displacement on the “ventriloquism” effect. Percept. Mot. Skills 37:967–79
    [Google Scholar]
  58. Jay MF, Sparks DL. 1984. Auditory receptive fields in primate superior colliculus shift with changes in eye position. Nature 309:345–47
    [Google Scholar]
  59. Jay MF, Sparks DL. 1987a. Sensorimotor integration in the primate superior colliculus. I. Motor convergence. J. Neurophysiol. 57:22–34
    [Google Scholar]
  60. Jay MF, Sparks DL. 1987b. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. J. Neurophysiol. 57:35–55
    [Google Scholar]
  61. Jenkins WM, Masterton RB. 1982. Sound localization: effects of unilateral lesions in central auditory system. J. Neurophysiol. 47:987–1016
    [Google Scholar]
  62. Kayser C. 2009. Phase resetting as a mechanism for supramodal attentional control. Neuron 64:300–2
    [Google Scholar]
  63. Kayser C, Petkov CI, Augath M, Logothetis NK. 2007. Functional imaging reveals visual modulation of specific fields in auditory cortex. J. Neurosci. 27:1824–35
    [Google Scholar]
  64. Kayser C, Petkov CI, Logothetis NK. 2008. Visual modulation of neurons in auditory cortex. Cereb. Cortex 18:1560–74
    [Google Scholar]
  65. Knudsen EI, Brainard MS. 1991. Visual instruction of the neural map of auditory space in the developing optic tectum. Science 253:85–87
    [Google Scholar]
  66. Knudsen EI, Knudsen PF. 1989. Vision calibrates sound localization in developing barn owls. J. Neurosci. 9:3306–13
    [Google Scholar]
  67. Knudsen EI, Knudsen PF. 1990. Sensitive and critical periods for visual calibration of sound localization by barn owls. J. Neurosci. 10:222–32
    [Google Scholar]
  68. Komura Y, Tamura R, Uwano T, Nishijo H, Ono T. 2005. Auditory thalamus integrates visual inputs into behavioral gains. Nat. Neurosci. 8:1203–9
    [Google Scholar]
  69. Kopco N, Lin IF, Shinn-Cunningham BG, Groh JM 2009. Reference frame of the ventriloquism aftereffect. J. Neurosci. 29:13809–14
    [Google Scholar]
  70. Kopco N, Loksa P, Lin IF, Groh J, Shinn-Cunningham B. 2019. Hemisphere-specific properties of the ventriloquism aftereffect. J. Acoust. Soc. Am. 146:EL177
    [Google Scholar]
  71. Kording KP, Beierholm U, Ma WJ, Quartz S, Tenenbaum JB, Shams L. 2007. Causal inference in multisensory perception. PLOS ONE 2:e943
    [Google Scholar]
  72. Lakatos P, O'Connell MN, Barczak A, Mills A, Javitt DC, Schroeder CE 2009. The leading sense: supramodal control of neurophysiological context by attention. Neuron 64:419–30
    [Google Scholar]
  73. Lee H, Noppeney U. 2014. Temporal prediction errors in visual and auditory cortices. Curr. Biol. 24:R309–10
    [Google Scholar]
  74. Lee J, Groh JM. 2012. Auditory signals evolve from hybrid- to eye-centered coordinates in the primate superior colliculus. J. Neurophysiol. 108:227–42
    [Google Scholar]
  75. Lee J, Groh JM. 2014. Different stimuli, different spatial codes: a visual map and an auditory rate code for oculomotor space in the primate superior colliculus. PLOS ONE 9:e85017
    [Google Scholar]
  76. MacSweeney M, Amaro E, Calvert GA, Campbell R, David AS et al. 2000. Silent speechreading in the absence of scanner noise: an event-related fMRI study. Neuroreport 11:1729–33
    [Google Scholar]
  77. Maier JX, Groh JM. 2010. Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates. Front. Integr. Neurosci. 4:121–32
    [Google Scholar]
  78. Martuzzi R, Murray MM, Michel CM, Thiran JP, Maeder PP et al. 2007. Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cereb. Cortex 17:1672–79
    [Google Scholar]
  79. Mascetti GG, Strozzi L. 1988. Visual cells in the inferior colliculus of the cat. Brain Res 442:387–90
    [Google Scholar]
  80. McAlpine D, Grothe B. 2003. Sound localization and delay lines—do mammals fit the model?. Trends Neurosci 26:347–50
    [Google Scholar]
  81. McGurk H, MacDonald J. 1976. Hearing lips and seeing voices. Nature 264:746–48
    [Google Scholar]
  82. Megevand P, Mercier MR, Groppe DM, Zion Golumbic E, Mesgarani N et al. 2020. Crossmodal phase reset and evoked responses provide complementary mechanisms for the influence of visual speech in auditory cortex. J. Neurosci. 40:8530–42
    [Google Scholar]
  83. Meredith MA, Stein BE. 1996. Spatial determinants of multisensory integration in cat superior colliculus neurons. J. Neurophysiol. 75:1843–57
    [Google Scholar]
  84. Metzger BA, Magnotti JF, Wang Z, Nesbitt E, Karas PJ et al. 2020. Responses to visual speech in human posterior superior temporal gyrus examined with iEEG deconvolution. J. Neurosci. 40:6938–48
    [Google Scholar]
  85. Middlebrooks JC, Clock AE, Xu L, Green DM. 1994. A panoramic code for sound location by cortical neurons. Science 264:842–44
    [Google Scholar]
  86. Mohl JT. 2020. Multisensory integration, segregation, and causal inference in the superior colliculus PhD Thesis, Duke Univ. Durham, NC:
    [Google Scholar]
  87. Mohl JT, Pearson JM, Groh JM. 2020. Monkeys and humans implement causal inference to simultaneously localize auditory and visual stimuli. J. Neurophysiol. 124:715–27
    [Google Scholar]
  88. Morrell F. 1972. Visual system's view of acoustic space. Nature 238:44–46
    [Google Scholar]
  89. Mottonen R, Krause CM, Tiippana K, Sams M. 2002. Processing of changes in visual speech in the human auditory cortex. Brain Res. Cogn. Brain Res. 13:417–25
    [Google Scholar]
  90. Murray MM, Thelen A, Thut G, Romei V, Martuzzi R, Matusz PJ. 2016. The multisensory function of the human primary visual cortex. Neuropsychologia 83:161–69
    [Google Scholar]
  91. Pages DS, Groh JM. 2013. Looking at the ventriloquist: visual outcome of eye movements calibrates sound localization. PLOS ONE 8:e72562
    [Google Scholar]
  92. Pages DS, Ross DA, Punal VM, Agashe S, Dweck I et al. 2016. Effects of electrical stimulation in the inferior colliculus on frequency discrimination by rhesus monkeys and implications for the auditory midbrain implant. J. Neurosci. 36:5071–83
    [Google Scholar]
  93. Paloff AM, Usunoff KG, Hinova-Palova DV, Ivanov DP 1985. Retinal innervation of the inferior colliculus in adult cats: electron microscopic observations. Neurosci. Lett. 54:339–44
    [Google Scholar]
  94. Pekkola J, Ojanen V, Autti T, Jääskeläinen IP, Möttönen R et al. 2005. Primary auditory cortex activation by visual speech: an fMRI study at 3 T. Neuroreport 16:125–28
    [Google Scholar]
  95. Populin LC, Tollin DJ, Yin TC. 2004. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat. J. Neurophysiol. 92:2151–67
    [Google Scholar]
  96. Porter KK, Metzger RR, Groh JM. 2006. Representation of eye position in primate inferior colliculus. J. Neurophysiol. 95:1826–42
    [Google Scholar]
  97. Porter KK, Metzger RR, Groh JM 2007. Visual- and saccade-related signals in the primate inferior colliculus. PNAS 104:17855–60
    [Google Scholar]
  98. Rebillard G, Carlier E, Rebillard M, Pujol R. 1977. Enhancement of visual responses on the primary auditory cortex of the cat after an early destruction of cochlear receptors. Brain Res 129:162–64
    [Google Scholar]
  99. Recanzone GH. 1998. Rapidly induced auditory plasticity: the ventriloquism aftereffect. PNAS 95:869–75
    [Google Scholar]
  100. Repérant J, Médina M, Ward R, Miceli D, Kenigfest NB et al. 2007. The evolution of the centrifugal visual system of vertebrates. A cladistic analysis and new hypotheses. Brain Res. Rev. 53:161–97
    [Google Scholar]
  101. Ress D, Chandrasekaran B. 2013. Tonotopic organization in the depth of human inferior colliculus. Front. Hum. Neurosci. 7:586
    [Google Scholar]
  102. Retter TL, Webster MA, Jiang F. 2019. Directional visual motion is represented in the auditory and association cortices of early deaf individuals. J. Cogn. Neurosci. 31:1126–40
    [Google Scholar]
  103. Rohe T, Noppeney U. 2015a. Cortical hierarchies perform Bayesian causal inference in multisensory perception. PLOS Biol 13:e1002073
    [Google Scholar]
  104. Rohe T, Noppeney U. 2015b. Sensory reliability shapes perceptual inference via two mechanisms. J. Vis. 15:22
    [Google Scholar]
  105. Rohe T, Noppeney U. 2016. Distinct computational principles govern multisensory integration in primary sensory and association cortices. Curr. Biol. 26:509–14
    [Google Scholar]
  106. Sams M, Aulanko R, Hämäläinen M, Hari R, Lounasmaa OV et al. 1991. Seeing speech: visual information from lip movements modifies activity in the human auditory cortex. Neurosci. Lett. 127:141–45
    [Google Scholar]
  107. Schroeder CE, Foxe JJ. 2002. The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. Brain Res. Cogn. Brain Res. 14:187–98
    [Google Scholar]
  108. Selezneva E, Gorkin A, Budinger E, Brosch M. 2018. Neuronal correlates of auditory streaming in the auditory cortex of behaving monkeys. Eur. J. Neurosci. 48:3234–45
    [Google Scholar]
  109. Shams L, Kamitani Y, Shimojo S. 2000. Illusions. What you see is what you hear. Nature 408:788
    [Google Scholar]
  110. Sur M, Garraghty PE, Roe AW. 1988. Experimentally induced visual projections into auditory thalamus and cortex. Science 242:1437–41
    [Google Scholar]
  111. Thurlow WR, Jack CE. 1973. Certain determinants of the “ventriloquism effect. .” Percept. Mot. Skills 36:1171–84
    [Google Scholar]
  112. Tsunada J, Liu AS, Gold JI, Cohen YE. 2016. Causal contribution of primate auditory cortex to auditory perceptual decision-making. Nat. Neurosci. 19:135–42
    [Google Scholar]
  113. Vachon P, Voss P, Lassonde M, Leroux JM, Mensour B et al. 2013. Reorganization of the auditory, visual and multimodal areas in early deaf individuals. Neuroscience 245:50–60
    [Google Scholar]
  114. von Melchner L, Pallas SL, Sur M. 2000. Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871–76
    [Google Scholar]
  115. Werner-Reiss U, Groh JM. 2008. A rate code for sound azimuth in monkey auditory cortex: implications for human neuroimaging studies. J. Neurosci. 28:3747–58
    [Google Scholar]
  116. Werner-Reiss U, Kelly KA, Trause AS, Underhill AM, Groh JM. 2003. Eye position affects activity in primary auditory cortex of primates. Curr. Biol. 13:554–62
    [Google Scholar]
  117. Willett SM, Groh JM, Maddox RK 2019. Hearing in a “moving” visual world: coordinate transformations along the auditory pathway. Multisensory Processes: The Auditory Perspectiveed. AK Lee, M Wallace, A Coffin, AN Popper, RR Faypp. 85–104 Berlin: Springer
    [Google Scholar]
  118. Woods TM, Lopez SE, Long JH, Rahman JE, Recanzone GH. 2006. Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J. Neurophysiol. 96:3323–37
    [Google Scholar]
  119. Wright TM, Pelphrey KA, Allison T, McKeown MJ, McCarthy G. 2003. Polysensory interactions along lateral temporal regions evoked by audiovisual speech. Cereb. Cortex 13:1034–43
    [Google Scholar]
  120. Yamauchi K, Yamadori T. 1982. Retinal projection to the inferior colliculus in the rat. Acta Anat 114:355–60
    [Google Scholar]
  121. Zella JC, Brugge JF, Schnupp JW. 2001. Passive eye displacement alters auditory spatial receptive fields of cat superior colliculus neurons. Nat. Neurosci. 4:1167–69
    [Google Scholar]
  122. Zhang AB. 1984. Retinotectal pathways in rodents: particularly from the retinal ganglion cells to the inferior colliculus. Taiwan Yi Xue Hui Za Zhi 83:1–8
    [Google Scholar]
  123. Zwiers MP, Versnel H, Van Opstal AJ. 2004. Involvement of monkey inferior colliculus in spatial hearing. J. Neurosci. 24:4145–56
    [Google Scholar]
/content/journals/10.1146/annurev-vision-091517-034003
Loading
/content/journals/10.1146/annurev-vision-091517-034003
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error