1932

Abstract

The superior colliculus is one of the most well-studied structures in the brain, and with each new report, its proposed role in behavior seems to increase in complexity. Forty years of evidence show that the colliculus is critical for reorienting an organism toward objects of interest. In monkeys, this involves saccadic eye movements. Recent work in the monkey colliculus and in the homologous optic tectum of the bird extends our understanding of the role of the colliculus in higher mental functions, such as attention and decision making. In this review, we highlight some of these recent results, as well as those capitalizing on circuit-based methodologies using transgenic mice models, to understand the contribution of the colliculus to attention and decision making. The wealth of information we have about the colliculus, together with new tools, provides a unique opportunity to obtain a detailed accounting of the neurons, circuits, and computations that underlie complex behavior.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-102016-061234
2017-09-15
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/vision/3/1/annurev-vision-102016-061234.html?itemId=/content/journals/10.1146/annurev-vision-102016-061234&mimeType=html&fmt=ahah

Literature Cited

  1. Adamuk E. 1870. Über die Innervation der Augenbewegungen. Zent. Med. Wiss 865 [Google Scholar]
  2. Albano JE, Norton TT, Hall WC. 1979. Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew. Tupaia glis. Brain Res. 173:1–11 [Google Scholar]
  3. Appell PP, Behan M. 1990. Sources of subcortical GABAergic projections to the superior colliculus of the cat. J. Comp. Neurol. 302:143–58 [Google Scholar]
  4. Apter JT. 1945. Projection of the retina on superior colliculus of cats. J. Neurophysiol. 8:123–34 [Google Scholar]
  5. Apter JT. 1946. Eye movements following strychninization of the superior colliculus of cats. J. Neurophysiol. 9:73–86 [Google Scholar]
  6. Asadollahi A, Mysore SP, Knudsen EI. 2010. Stimulus-driven competition in a cholinergic midbrain nucleus. Nat. Neurosci. 13:889–95 [Google Scholar]
  7. Baginskas A, Kuraite V, Kuras A. 2011. Presynaptic nicotinic potentiation of a frog retinotectal transmission evoked by discharge of a single retina ganglion cell. Neurosci. Res. 70:391–400 [Google Scholar]
  8. Baginskas A, Kuraite V, Kuras A. 2012. Phasic nicotinic potentiation of frog retinotectal transmission enhances intrinsic activity of tectum column. Neurosci. Res. 74:42–47 [Google Scholar]
  9. Baro JA, Hughes HC, Peck CK. 1995. Express saccades in cat: effects of task and target modality. Exp. Brain Res. 103:209–17 [Google Scholar]
  10. Basso MA, Sommer MA. 2011. Exploring the role of the substantia nigra pars reticulata in eye movements. Neuroscience 198:205–12 [Google Scholar]
  11. Basso MA, Wurtz RH. 1997. Modulation of neuronal activity by target uncertainty. Nature 389:66–69 [Google Scholar]
  12. Basso MA, Wurtz RH. 1998. Modulation of neuronal activity in superior colliculus by changes in target probability. J. Neurosci. 18:7519–34 [Google Scholar]
  13. Basso MA, Wurtz RH. 2002. Neuronal activity in substantia nigra pars reticulata during target selection. J. Neurosci. 22:1883–94 [Google Scholar]
  14. Behan M, Appell PP. 1992. Intrinsic circuitry in the cat superior colliculus: projections from the superficial layers. J. Comp. Neurol. 315:230–43 [Google Scholar]
  15. Bickford ME, Hall WC. 1992. The nigral projection to predorsal bundle cells in the superior colliculus of the rat. J. Comp. Neurol. 319:11–33 [Google Scholar]
  16. Bickford ME, Zhau N, Krahe TE, Govindaiah G, Guido W. 2015. Retinal and tectal “driver-like” inputs converge in the shell of the mouse lateral geniculate nucleus. J. Neurosci. 35:10523–34 [Google Scholar]
  17. Binns KE, Salt TE. 1997. Different roles for GABAA and GABAB receptors in visual processing in the rat superior colliculus. J. Physiol. 504:629–39 [Google Scholar]
  18. Boch R, Fischer B, Ramsperger E. 1984. Express-saccades of the monkey: reaction times versus intensity, size, duration and eccentricity of their targets. Exp. Brain Res. 55:223–31 [Google Scholar]
  19. Borra E, Gerbella M, Rozzi S, Tonelli S, Luppino G. 2014. Projections to the superior colliculus from inferior parietal, ventral premotor, and ventrolateral prefrontal areas involved in controlling goal-directed hand actions in the macaque. Cereb. Cortex 24:1054–65 [Google Scholar]
  20. Bowling DB, Michael CR. 1980. Projection patterns of single physiologically characterized optic tract fibres in cat. Nature 286:899–902 [Google Scholar]
  21. Boynton GM. 2009. A framework for describing the effects of attention on visual responses. Vis. Res. 49:1129–43 [Google Scholar]
  22. Brecht M, Singer W, Engel AK. 2004. Amplitude and direction of saccadic eye movements depend on the synchronicity of collicular population activity. J. Neurophysiol. 92:424–32 [Google Scholar]
  23. Butler BE, Chabot N, Lomber SG. 2016. A quantitative comparison of the hemispheric, areal, and laminar origins of sensory and motor cortical projections to the superior colliculus of the cat. J. Comp. Neurol. 524:2623–42 [Google Scholar]
  24. Carandini M, Heeger DJ. 2012. Normalization as a canonical neural computation. Nat. Rev. Neurosci. 13:51–62 [Google Scholar]
  25. Carello CD, Krauzlis RJ. 2004. Manipulating intent: evidence for a causal role of the superior colliculus in target selection. Neuron 43:575–83 [Google Scholar]
  26. Casagrande VA, Diamond IT. 1974. Ablation study of the superior colliculus in the tree shrew (Tupaia glis).. J. Comp. Neurol. 156:207–37 [Google Scholar]
  27. Casagrande VA, Harting JK, Hall WC, Diamond IT, Martin GF. 1972. Superior colliculus of the tree shrew: a structural and functional subdivision into superficial and deep layers. Science 177:444–47 [Google Scholar]
  28. Cavanaugh J, Alvarez BD, Wurtz RH. 2006. Enhanced performance with brain stimulation: attentional shift or visual cue?. J. Neurosci. 26:11347–58 [Google Scholar]
  29. Cavanaugh J, Wurtz RH. 2004. Subcortical modulation of attention counters change blindness. J. Neurosci. 24:11236–43 [Google Scholar]
  30. Chalupa LM, Rhoades RW. 1977. Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus. J. Physiol. 270:595–626 [Google Scholar]
  31. Chevalier G, Deniau JM, Thierry AM, Feger J. 1981. The nigro-tectal pathway. An electrophysiological reinvestigation in the rat. Brain Res 213:253–63 [Google Scholar]
  32. Clower DM, West RA, Lynch JC, Strick PL. 2001. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J. Neurosci. 21:6283–91 [Google Scholar]
  33. Colby CL, Goldberg ME. 1999. Space and attention in parietal cortex. Annu. Rev. Neurosci. 23:319–49 [Google Scholar]
  34. Corneil BD, Olivier E, Munoz DP. 2002. Neck muscle responses to stimulation of monkey superior colliculus. II. Gaze shift initiation and volitional head movements. J. Neurophysiol. 88:2000–18 [Google Scholar]
  35. Courjon J-H, Zénon A, Clément G, Urquizar C, Olivier E, Pélisson D. 2015. Electrical stimulation of the superior colliculus induces non-topographically organized perturbation of reaching movements in cats. Front. Syst. Neurosci. 9:109 [Google Scholar]
  36. Crapse TB, Basso MA. 2014. Sensory priming influences form-based perceptual decision-making and superior colliculus population activity Presented at Annu. Meet. Soc. for Neurosci., Nov. 15–19 Washington, DC:
  37. Dean P, Redgrave P, Westby GW. 1989. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137–47 [Google Scholar]
  38. Deniau JM, Chevalier G. 1992. The lamellar organization of the rat substantia nigra pars reticulata: distribution of projection neurons. Neuroscience 46:361 [Google Scholar]
  39. Deubel H, Schneider WX. 1996. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vis. Res. 36:1827–37 [Google Scholar]
  40. Drager UC, Hubel DH. 1975. Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. J. Neurophysiol. 38:690–713 [Google Scholar]
  41. Dunn CA, Colby CL. 2010. Representation of the ipsilateral visual field by neurons in the macaque lateral intraparietal cortex depends on the forebrain commissures. J. Neurophysiol. 104:2624–33 [Google Scholar]
  42. Dunn CA, Hall NJ, Colby CL. 2010. Spatial updating in monkey superior colliculus in the absence of the forebrain commissures: dissociation between superficial and intermediate layers. J. Neurophysiol. 104:1267–85 [Google Scholar]
  43. Edelman JA, Goldberg ME. 2001. Dependence of saccade-related activity in the primate superior colliculus on visual target presence. J. Neurophysiol. 86:676–91 [Google Scholar]
  44. Edelman JA, Goldberg ME. 2003. Saccade-related activity in the primate superior colliculus depends on the presence of local landmarks at the saccade endpoint. J. Neurophysiol. 90:1728–36 [Google Scholar]
  45. Edelman JA, Keller EL. 1998. Dependence on target configuration of express saccade-related activity in the primate superior colliculus. J. Neurophysiol. 80:1407–26 [Google Scholar]
  46. Edwards S. 1980. The deep cell layers of the superior colliculus: their reticular characteristics and structural organization. The Reticular Formation Revisited JA Hobson, MAB Brazier 193–209 New York: Raven Press [Google Scholar]
  47. Edwards SB, Ginsburgh CL, Henkel CK, Stein BE. 1979. Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neurol. 184:309–30 [Google Scholar]
  48. Egeth HE, Yantis S. 1997. Visual attention: control, representation, and time course. Annu. Rev. Psychol. 48:269–97 [Google Scholar]
  49. Endo T, Isa T. 2001. Functionally different AMPA-type glutamate receptors in morphologically identified neurons in rat superficial superior colliculus. Neuroscience 108:129–41 [Google Scholar]
  50. Endo T, Yanagawa Y, Obata K, Isa T. 2005. Nicotinic acetylcholine receptor subtypes involved in facilitation of GABAergic inhibition in mouse superficial superior colliculus. J. Neurophysiol. 94:3893–902 [Google Scholar]
  51. Feinberg EH, Meister M. 2015. Orientation columns in the mouse superior colliculus. Nature 519:229–32 [Google Scholar]
  52. Felsen G, Mainen ZF. 2008. Neural substrates of sensory-guided locomotor decisions in the rat superior colliculus. Neuron 60:137–48 [Google Scholar]
  53. Findlay JM. 1982. Global visual processing for saccadic eye movements. Vis. Res. 22:1033–45 [Google Scholar]
  54. Fischer B, Ramsperger E. 1984. Human express-saccades: extremely short reaction times of goal directed eye movements. Exp. Brain Res. 57:191–95 [Google Scholar]
  55. Fuchs AF, Robinson DA. 1966. A method for measuring horizontal and vertical eye movement chronically in the monkey. J. Appl. Physiol. 21:1068–70 [Google Scholar]
  56. Gale SD, Murphy GJ. 2014. Distinct representation and distribution of visual information by specific cell types in mouse superficial superior colliculus. J. Neurosci. 34:13458–71 [Google Scholar]
  57. Gale SD, Murphy GJ. 2016. Active dendritic properties and local inhibitory input enable selectivity for object motion in mouse superior colliculus neurons. J. Neurosci. 36:9111–23 [Google Scholar]
  58. Gattass R, Desimone R. 1996. Responses of cells in the superior colliculus during performance of a spatial attention task in the macaque. Rev. Bras. Biol. 56:257–79 [Google Scholar]
  59. Ghitani N, Bayguinov PO, Basso MA, Jackson MB. 2016. A sodium afterdepolarization in rat superior colliculus neurons and its contribution to population activity. J. Neurophysiol. 116:191–200 [Google Scholar]
  60. Ghitani N, Bayguinov PO, Vokoun CR, McMahon S, Jackson MB, Basso MA. 2014. Excitatory synaptic feedback from the motor layer to the sensory layers of the superior colliculus. J. Neurosci. 34:6822–33 [Google Scholar]
  61. Ghose D, Maier A, Nidiffer A, Wallace MT. 2014. Multisensory response modulation in the superficial layers of the superior colliculus. J. Neurosci. 34:4332–44 [Google Scholar]
  62. Glimcher PW, Sparks DL. 1992. Movement selection in advance of action in the superior colliculus. Nature 355:542–45 [Google Scholar]
  63. Glimcher PW, Sparks DL. 1993. Representation of averaging saccades in the superior colliculus of the monkey. Exp. Brain Res. 95:429–35 [Google Scholar]
  64. Gnadt JW, Bracewell RM, Andersen RA. 1991. Sensorimotor transformation during eye movements to remembered visual targets. Vis. Res. 31:693–715 [Google Scholar]
  65. Goddard CA, Mysore SP, Bryant AS, Huguenard JR, Knudsen EI. 2014. Spatially reciprocal inhibition of inhibition within a stimulus selection network in the avian midbrain. PLOS ONE 9:e85865 [Google Scholar]
  66. Goddard CA, Sridharan D, Huguenard JR, Knudsen EI. 2012. Gamma oscillations are generated locally in an attention-related midbrain network. Neuron 73:567–80 [Google Scholar]
  67. Goldberg ME, Wurtz RH. 1972a. Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. J. Neurophysiol. 35:542–59 [Google Scholar]
  68. Goldberg ME, Wurtz RH. 1972b. Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. J. Neurophysiol. 35:560–74 [Google Scholar]
  69. Graham J, Lin C-S, Kaas JH. 1979. Subcortical projections of six visual cortical areas in the owl monkey. Aotus trivirgatus. J. Comp. Neurol. 187:557–80 [Google Scholar]
  70. Graybiel AM. 1978. A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers. Brain Res 145:365–74 [Google Scholar]
  71. Green DM, Swets JA. 1966. Signal Detection Theory and Psychophysics New York: Wiley
  72. Groh JM, Sparks DL. 1996. Saccades to somatosensory targets. II. Motor convergence in primate superior colliculus. J. Neurophysiol. 75:428–38 [Google Scholar]
  73. Gupta A, Wang Y, Markram H. 2000. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273–78 [Google Scholar]
  74. Hafed ZM, Chen C-Y. 2016. Sharper, stronger, faster upper visual field representation in primate superior colliculus. Curr. Biol. 26:1647–58 [Google Scholar]
  75. Hall NJ, Colby CL. 2016. Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast. PNAS 113:6743–48 [Google Scholar]
  76. Hall WC, Fitzpatrick D, Klatt LL, Raczkowski D. 1989. Cholinergic innervation of the superior colliculus in the cat. J. Comp. Neurol. 287:495–514 [Google Scholar]
  77. Harting JK. 1977. Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J. Comp. Neurol. 173:583–612 [Google Scholar]
  78. Harting JK, Feig S, Van Lieshout DP. 1997. Cortical somatosensory and trigeminal inputs to the cat superior colliculus: light and electron microscopic analyses. J. Comp. Neurol. 38:313–26 [Google Scholar]
  79. Harting JK, Huerta MF, Hashikawa T, van Lieshout DP. 1991. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304:275–306 [Google Scholar]
  80. Harting JK, Updyke BV, Van Lieshout DP. 1992. Corticotectal projections in the cat: anterograde transport studies of twenty-five cortical areas. J. Comp. Neurol. 324:379–414 [Google Scholar]
  81. Helms MC, Ozen G, Hall WC. 2004. Organization of the intermediate gray layer of the superior colliculus. I. Intrinsic vertical connections. J. Neurophysiol. 91:1706–15 [Google Scholar]
  82. Hemelt ME, Keller A. 2008. Superior colliculus control of vibrissa movements. J. Neurophysiol. 100:1245–54 [Google Scholar]
  83. Hess WR, Burgi S, Bucher V. 1946. Motorisch Funktion des Tektal und Temgentalgebietes. Monatsschr. Psychiatr. Neurol. 112:1–52 [Google Scholar]
  84. Hikosaka O, Takikawa Y, Kawagoe R. 2000. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80:953–78 [Google Scholar]
  85. Hikosaka O, Wurtz RH. 1985. Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. J. Neurophysiol. 53:266–91 [Google Scholar]
  86. Hormigo S, Vega-Flores G, Castro-Alamancos MA. 2016. Basal ganglia output controls active avoidance behavior. J. Neurosci. 36:10274–84 [Google Scholar]
  87. Horwitz GD, Batista AP, Newsome WT. 2004. Representation of an abstract perceptual decision in macaque superior colliculus. J. Neurophysiol. 91:2281 [Google Scholar]
  88. Horwitz GD, Newsome WT. 1999. Separate signals for target selection and movement specification in the superior colliculus. Science 284:1158–61 [Google Scholar]
  89. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA. 2009. Genetic identification of an on-off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62:327 [Google Scholar]
  90. Huerta MF, Harting JK. 1984. The mammalian superior colliculus: studies of its morphology and connections. Comparative Neurology of the Optic Tectum H Vanegas 687–773 New York: Plenum Publ. [Google Scholar]
  91. Illing R-B, Graybiel AM. 1985. Convergence of afferents from frontal cortex and substantia nigra onto acetylcholinesterase-rich patches of the cat's superior colliculus. Neuroscience 14:455–82 [Google Scholar]
  92. Illing R-B, Graybiel AM. 1986. Complementary and non-matching afferent compartments in the cat's superior colliculus: innervation of the acetylcholinesterase-poor domain of the intermediate gray layer. Neuroscience 18:373 [Google Scholar]
  93. Illing R-B, Vogt DM, Spatz WB. 1990. Parvalbumin in rat superior colliculus. Neurosci. Lett. 120:197 [Google Scholar]
  94. Isa T. 2002. Intrinsic processing in the mammalian superior colliculus. Curr. Opin. Neurobiol. 12:668 [Google Scholar]
  95. Isa T, Endo T, Saito Y. 1998. The visuo-motor pathway in the local circuit of the rat superior colliculus. J. Neurosci. 18:8496–504 [Google Scholar]
  96. Isa T, Hall WC. 2009. Exploring the superior colliculus in vitro. J. Neurophysiol. 102:2581–93 [Google Scholar]
  97. Itti L, Koch C. 2000. A saliency-based search mechanism for overt and covert shifts of visual attention. Vis. Res. 40:1489–506 [Google Scholar]
  98. Jay MF, Sparks DL. 1984. Auditory receptive fields in primate superior colliculus shift with changes in eye position. Nature 309:345–47 [Google Scholar]
  99. Kaneda K, Phongphanphanee P, Katoh T, Isa K, Yanagawa Y. et al. 2008. Regulation of burst activity through presynaptic and postsynaptic GABAB receptors in mouse superior colliculus. J. Neurosci. 28:816–27 [Google Scholar]
  100. Kardamakis AA, Saitoh K, Grillner S. 2015. Tectal microcircuit generating visual selection commands on gaze-controlling neurons. PNAS 112:E1956–65 [Google Scholar]
  101. Karten HJ, Dubbeldam JL. 1973. The organization and projections of the paleostriatal complex in the pigeon (columba livia). J. Comp. Neurol. 148:61–89 [Google Scholar]
  102. Kastner S, Ungerleider LG. 2000. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23:315–41 [Google Scholar]
  103. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7:476–86 [Google Scholar]
  104. Kim B, Basso MA. 2008. Saccade target selection in the superior colliculus: a signal detection theory approach. J. Neurosci. 28:2991–3007 [Google Scholar]
  105. Kim B, Basso MA. 2010. A probabilistic strategy for understanding action selection. J. Neurosci. 30:2340–55 [Google Scholar]
  106. King WM. 1990. Nicotinic depolarization of optic nerve terminals augments synaptic transmission. Brain Res 527:150–54 [Google Scholar]
  107. Klier EM, Wang H, Crawford JD. 2001. The superior colliculus encodes gaze commands in retinal coordinates. Nat. Neurosci. 4:627–32 [Google Scholar]
  108. Knudsen EI. 1982. Auditory and visual maps of space in the optic tectum of the owl. J. Neurosci. 2:1177–94 [Google Scholar]
  109. Knudsen EI. 2011. Control from below: the role of a midbrain network in spatial attention. Eur. J. Neurosci. 33:1961–72 [Google Scholar]
  110. Knudsen EI, Brainard MS. 1991. Visual instruction of the neural map of auditory space in the developing optic tectum. Science 253:86–87 [Google Scholar]
  111. Koch C, Ullman S. 1985. Shifts in selective visual attention: towards the underlying neural circuitry. Hum. Neurobiol. 4:219–27 [Google Scholar]
  112. Kowler E, Anderson E, Dosher B, Blaser E. 1995. The role of attention in the programming of saccades. Vis. Res. 35:1897–916 [Google Scholar]
  113. Kowler E, Blaser E. 1995. The accuracy and precision of saccades to small and large targets. Vis. Res. 35:1741–54 [Google Scholar]
  114. Krauzlis RJ, Basso MA, Wurtz RH. 2000. Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. J. Neurophysiol. 84:876–91 [Google Scholar]
  115. Krauzlis RJ, Bollimunta A, Arcizet F, Wang L. 2014. Attention as an effect not a cause. Trends Cogn. Sci. 18:457–64 [Google Scholar]
  116. Krauzlis RJ, Dill N. 2002. Neural correlates of target choice for pursuit and saccades in the primate superior colliculus. Neuron 35:355–63 [Google Scholar]
  117. Krauzlis RJ, Lovejoy LP, Zénon A. 2013. Superior colliculus and visual spatial attention. Annu. Rev. Neurosci. 36:165–82 [Google Scholar]
  118. Langer TP, Lund RD. 1974. The upper layers of the superior colliculus of the rat: a Golgi study. J. Comp. Neurol. 158:405–35 [Google Scholar]
  119. Lee J, Maunsell JH. 2009. A normalization model of attentional modulation of single unit responses. PLOS ONE 4:e4651 [Google Scholar]
  120. Lee P, Hall WC. 1995. Interlaminar connections of the superior colliculus in the tree shrew. II: projections from the superficial gray to the optic layer. Vis. Neurosci. 12:573–88 [Google Scholar]
  121. Lee P, Hall WC. 2006. An in vitro study of horizontal connections in the intermediate layer of the superior colliculus. J. Neurosci. 26:4763–68 [Google Scholar]
  122. Lee PH, Helms MC, Augustine GJ, Hall WC. 1997. Role of intrinsic synaptic circuitry in collicular sensorimotor integration. PNAS 94:13299–304 [Google Scholar]
  123. Lee PH, Schmidt M, Hall WC. 2001. Excitatory and inhibitory circuitry in the superficial gray layer of the superior colliculus. J. Neurosci. 21:8145–53 [Google Scholar]
  124. Lee PH, Sooksawate T, Yanagawa Y, Isa K, Isa T, Hall WC. 2007. Identity of a pathway for saccadic suppression. PNAS 104:6824–27 [Google Scholar]
  125. Li X, Basso MA. 2005. Competitive stimulus interactions within single response fields of superior colliculus neurons. J. Neurosci. 25:11357–73 [Google Scholar]
  126. Li X, Basso MA. 2008. Preparing to move increases the sensitivity of superior colliculus neurons. J. Neurosci. 28:4561–77 [Google Scholar]
  127. Lo C-C, Wang X-J. 2006. Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nat. Neurosci. 9:956 [Google Scholar]
  128. Lovejoy LP, Krauzlis RJ. 2010. Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat. Neurosci. 13:261–66 [Google Scholar]
  129. Luo TZ, Maunsell JHR. 2015. Neuronal modulations in visual cortex are associated with only one of multiple components of attention. Neuron 86:1182–88 [Google Scholar]
  130. Lyon DC, Nassi JJ, Callaway EM. 2010. A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. Neuron 65:270–79 [Google Scholar]
  131. Ma WJ, Beck JM, Latham PE, Pouget A. 2006. Bayesian inference with probabilistic population codes. Nat. Neurosci 9:1432 [Google Scholar]
  132. Mana S, Chevalier G. 2001. The fine organization of nigro-collicular channels with additional observations of their relationships with acetylcholinesterase in the rat. Neuroscience 106:357 [Google Scholar]
  133. Marín G, Mpdozis J, Sentis E, Ossandón T, Letelier JC. 2005. Oscillatory bursts in the optic tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis. J. Neurosci. 25:7081–89 [Google Scholar]
  134. Marín G, Salas C, Sentis E, Rojas X, Letelier JC, Mpodozis J. 2007. A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J. Neurosci. 27:8112–21 [Google Scholar]
  135. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5:793–807 [Google Scholar]
  136. Maunsell JHR. 2015. Neuronal mechanisms of visual attention. Annu. Rev. Vis. Sci. 1:373–91 [Google Scholar]
  137. May PJ. 2006. The mammalian superior colliculus: laminar structure and connections. Prog. Brain Res. 151:321–78 [Google Scholar]
  138. Mays LE, Sparks DL. 1980. Dissociation of visual and saccade-related responses in superior colliculus neurons. J. Neurophysiol. 43:207–32 [Google Scholar]
  139. McAdams CJ, Maunsell JHR. 1999. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19:431–41 [Google Scholar]
  140. McGowan JW, Kowler E, Sharma A, Chubb C. 1998. Saccadic localization of random dot targets. Vis. Res. 38:895 [Google Scholar]
  141. McHaffie JG, Stanford TR, Stein BE, Coizet V, Redgrave P. 2005. Subcortical loops through the basal ganglia. Trends Neurosci 28:401–7 [Google Scholar]
  142. McHaffie JG, Stein BE. 1982. Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247:243–53 [Google Scholar]
  143. McIlwain JT. 1986. Point images in the visual system: new interest in an old idea. Trends Neurosci 9:354–58 [Google Scholar]
  144. McIlwain JT. 1991. Distributed spatial coding in the superior colliculus: a review. Vis. Neurosci. 6:3–13 [Google Scholar]
  145. McPeek RM, Keller EL. 2004. Deficits in saccade target selection after inactivation of superior colliculus. Nat. Neurosci. 7:757–63 [Google Scholar]
  146. Melcher D, Kowler E. 1999. Shapes, surfaces and saccades. Vis. Res. 39:2929 [Google Scholar]
  147. Middlebrooks J, Knudsen E. 1984. A neural code for auditory space in the cat's superior colliculus. J. Neurosci. 4:2621–34 [Google Scholar]
  148. Mooney RD, Nikoletseas MM, Hess PR, Allen Z, Lewin AC, Rhoades RW. 1988a. The projection from the superficial to the deep layers of the superior colliculus: an intracellular horseradish peroxidase injection study in the hamster. J. Neurosci. 8:1384–99 [Google Scholar]
  149. Mooney RD, Nikoletseas MM, Ruiz SA, Rhoades RW. 1988b. Receptive-field properties and morphological characteristics of the superior collicular neurons that project to the lateral posterior and dorsal lateral geniculate nuclei in the hamster. J. Neurophysiol. 59:1333–51 [Google Scholar]
  150. Moschovakis AK, Highstein SM. 1994. The anatomy and physiology of primate neurons that control rapid eye movements. Annu. Rev. Neurosci. 17:465–88 [Google Scholar]
  151. Moschovakis AK, Karabelas AB, Highstein SM. 1988a. Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. J. Neurophysiol. 60:232–62 [Google Scholar]
  152. Moschovakis AK, Karabelas AB, Highstein SM. 1988b. Structure-function relationships in the primate superior colliculus. II. Morphological identification of presaccadic neurons. J. Neurophysiol. 60:263–302 [Google Scholar]
  153. Müller JR, Philiastides MG, Newsome WT. 2005. Microstimulation of the superior colliculus focuses attention without moving the eyes. PNAS 102:524–29 [Google Scholar]
  154. Munoz DP, Wurtz RH. 1995. Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol. 73:2313–33 [Google Scholar]
  155. Mysore SP, Knudsen EI. 2014. Descending control of neural bias and selectivity in a spatial attention network: rules and mechanisms. Neuron 84:214–26 [Google Scholar]
  156. Ni AM, Ray S, Maunsell JHR. 2012. Tuned normalization explains the size of attention modulations. Neuron 73:803–13 [Google Scholar]
  157. Nummela SU, Krauzlis RJ. 2010. Inactivation of primate superior colliculus biases target choice for smooth pursuit, saccades, and button press responses. J. Neurophysiol. 104:1538–48 [Google Scholar]
  158. Ottes FP, Van Gisbergen JA, Eggermont JJ. 1984. Metrics of saccade responses to visual double stimuli: two different modes. Vis. Res. 24:1169–79 [Google Scholar]
  159. Özen G, Helms MC, Hall WC. 2004. The intracollicular neuronal network. The Superior Colliculus: New Approaches for Studying Sensorimotor Integration WC Hall, A Moschovakis 147–58 Boca Raton, FL: CRC Press [Google Scholar]
  160. Palmer AR, King AJ. 1982. The representation of auditory space in the mammalian superior colliculus. Nature 299:248–49 [Google Scholar]
  161. Pélisson D, Guitton D, Munoz DP. 1991. Superior colliculus and feedback control of gaze shift in the head-free cat. Oculomotor Control and Cognitive Processes R Schmid, D Zambarbieri 213–28 Amsterdam: Elsevier Sci. Publ. B.V. [Google Scholar]
  162. Phongphanphanee P, Mizuno F, Lee PH, Yanagawa Y, Isa T, Hall WC. 2011. A circuit model for saccadic suppression in the superior colliculus. J. Neurosci. 31:1949–54 [Google Scholar]
  163. Pi H-J, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A. 2013. Cortical interneurons that specialize in disinhibitory control. Nature 503:521–24 [Google Scholar]
  164. Port NL, Wurtz RH. 2003. Sequential activity of simultaneously recorded neurons in the superior colliculus during curved saccades. J. Neurophysiol. 90:1887–903 [Google Scholar]
  165. Pouget A, Dayan P, Zemel RS. 2003. Inference and computation with population codes. Annu. Rev. Neurosci. 26:381–410 [Google Scholar]
  166. Pouget A, Deneve S, Ducom J-C, Latham P. 1999. Narrow versus wide tuning curves: What's best for a population code?. Neural Comp 11:85–90 [Google Scholar]
  167. Prescott IA, Dostrovsky JO, Moro E, Hodaie M, Lozano AM, Hutchison WD. 2008. Levodopa enhances synaptic plasticity in the substantia nigra pars reticulata of Parkinson's disease patients. Brain 132:309–18 [Google Scholar]
  168. Ray S, Maunsell JHR. 2015. Do gamma oscillations play a role in cerebral cortex. ? Trends Cogn. Sci. 19:78–85 [Google Scholar]
  169. Redgrave P, Prescott TJ, Gurney K. 1999. The basal ganglia: the vertebrate solution to the selection problem?. Neuroscience 89:1009–23 [Google Scholar]
  170. Reynolds JH, Chelazzi L. 2004. Attentional modulation of visual processing. Annu. Rev. Neurosci. 27:611–47 [Google Scholar]
  171. Reynolds JH, Heeger DJ. 2009. The normalization model of attention. Neuron 61:168–85 [Google Scholar]
  172. Rhoades RW, Mooney RD, Rohrer WH, Nikoletseas MM, Fish SE. 1989. Organization of the projection from the superficial to the deep layers of the hamster's superior colliculus as demonstrated by the anterograde transport of Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 283:54–70 [Google Scholar]
  173. Rizzolatti G, Camarda R, Grupp LA, Pisa M. 1973. Inhibition of visual responses of single units in the cat superior colliculus by the introduction of a second visual stimulus. Brain Res 61:390–94 [Google Scholar]
  174. Rizzolatti G, Camarda R, Grupp LA, Pisa M. 1974. Inhibitory effect of remote visual stimuli on visual response of cat superior colliculus: spatial and temporal factors. J. Neurophysiol. 37:1262–75 [Google Scholar]
  175. Rizzolatti G, Riggio L, Dascola I, Umiltá C. 1987. Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25:31–40 [Google Scholar]
  176. Robinson DA. 1972. Eye movements evoked by collicular stimulation in the alert monkey. Vis. Res. 12:1795–808 [Google Scholar]
  177. Rodgers CK, Munoz DP, Scott SH, Pare M. 2006. Discharge properties of monkey tectoreticular neurons. J. Neurophysiol. 95:3502–11 [Google Scholar]
  178. Roitman JD, Shadlen MN. 2002. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22:9475–89 [Google Scholar]
  179. Roll A, Wierzbicka MM, Wolf W. 1996. The “gap paradigm” leads to express-like saccadic reaction times in Parkinson's disease. Exp. Brain Res. 111:131–38 [Google Scholar]
  180. Rowland BA, Stein BE. 2014. A model of the temporal dynamics of multisensory enhancement. Neurosci. Biobehav. Rev. 41:78–84 [Google Scholar]
  181. Sachs GM, Schneider GE. 1984. The morphology of optic tract axons arborizing in the superior colliculus of the hamster. J. Comp. Neurol. 230:155–67 [Google Scholar]
  182. Saito Y, Isa T. 1999. Electrophysiological and morphological properties of neurons in the rat superior colliculus. I. Neurons in the intermediate layers. J. Neurophysiol. 82:754–67 [Google Scholar]
  183. Saito Y, Isa T. 2003. Local excitatory network and NMDA receptor activation generate a synchronous and bursting command from the superior colliculus. J. Neurosci. 23:5854–64 [Google Scholar]
  184. Schiller PH. 1984. The superior colliculus and visual function. Handbook of Physiology JM Brookhart, VB Mountcastle, pp. 457–505 Philadelphia: Lippincott Williams and Wilkins [Google Scholar]
  185. Schiller PH, Stryker M. 1972. Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 35:915–24 [Google Scholar]
  186. Schiller PH, Stryker M, Cynader M, Berman N. 1974. Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. J. Neurophysiol. 37:181–94 [Google Scholar]
  187. Sereno MI, Ulinski PS. 1987. Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle, Pseudemys scripta. J. Comp. Neurol. 261:319–46 [Google Scholar]
  188. Shang C, Liu Z, Chen Z, Shi Y, Wang Q. et al. 2015. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 348:1472–77 [Google Scholar]
  189. Sheliga BM, Riggio L, Rizzolatti G. 1994. Orienting of attention and eye movements. Exp. Brain Res. 98:507–22 [Google Scholar]
  190. Sheliga BM, Riggio L, Rizzolatti G. 1995. Spatial attention and eye movements. Exp. Brain Res. 105:261–75 [Google Scholar]
  191. Sohal VS. 2012. Insights into cortical oscillations arising from optogenetic studies. Biol. Psychiatry 71:1039–45 [Google Scholar]
  192. Sohal VS, Zhang F, Yizhar O, Deisseroth K. 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698–702 [Google Scholar]
  193. Sommer MA. 1994. Express saccades elicited during visual scan in the monkey. Vis. Res. 34:2023–38 [Google Scholar]
  194. Sparks DL. 1975. Response properties of eye movement-related neurons in the monkey superior colliculus. Brain Res 90:147–52 [Google Scholar]
  195. Sparks DL. 1978. Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain Res 156:1–16 [Google Scholar]
  196. Sparks DL. 1988. Neural cartography: sensory and motor maps in the superior colliculus. Brain Behav. Evol. 31:49–56 [Google Scholar]
  197. Sparks DL, Hartwich-Young R. 1989. The deep layers of the superior colliculus. Rev. Oculomot. Res. 3:213–55 [Google Scholar]
  198. Sparks DL, Mays LE. 1990. Signal transformations required for the generation of saccadic eye movements. Annu. Rev. Neurosci. 13:309–36 [Google Scholar]
  199. Spitzer H, Desimone R, Moran J. 1988. Increased attention enhances both behavioral and neuronal performance. Science 240:338–40 [Google Scholar]
  200. Stanford TR, Freedman EG, Sparks DL. 1996. Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J. Neurophysiol. 76:3360–81 [Google Scholar]
  201. Stein BE, Clamann HP. 1981. Control of pinna movements and sensorimotor register in cat superior colliculus. Brain Behav. Evol. 19:180–92 [Google Scholar]
  202. Stein BE, Meredith MA. 1993. The Merging of the Senses Cambridge, MA: MIT Press
  203. Syka J, Radil-Weiss T. 1971. Electrical stimulation of the tectum in freely moving cats. Brain Res 28:567–72 [Google Scholar]
  204. Tamamaki N, Uhlrich DJ, Sherman SM. 1995. Morphology of physiologically identified retinal X and Y axons in the cat's thalamus and midbrain as revealed by intraaxonal injection of biocytin. J. Comp. Neurol. 354:583–607 [Google Scholar]
  205. Taniguchi H. 2014. Genetic dissection of GABAergic neural circuits in mouse neocortex. Front. Cell. Neurosci. 8:8 [Google Scholar]
  206. Taniguchi H, He M, Wu P, Kim S, Paik R. et al. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995–1013 [Google Scholar]
  207. Tardif E, Delacuisine B, Probst A, Clarke S. 2005. Intrinsic connectivity of human superior colliculus. Exp. Brain Res. 166:316–24 [Google Scholar]
  208. Tehovnik EJ, Yeomans JS. 1986. Two converging brainstem pathways mediating circling behavior. Brain Res 385:329–42 [Google Scholar]
  209. Thevarajah D, Mikulic A, Dorris MC. 2009. Role of the superior colliculus in choosing mixed-strategy saccades. J. Neurosci. 29:1998–2008 [Google Scholar]
  210. Titmus MJ, Tsai HJ, Lima R, Udin SB. 1999. Effects of choline and other nicotinic agonists on the tectum of juvenile and adult Xenopus frogs: a patch-clamp study. Neuroscience 91:753–69 [Google Scholar]
  211. Van Opstal AJ, Van Gisbergen JAM, Smit AC. 1990. Comparison of saccades evoked by visual stimulation and collicular electrical stimulation in the alert monkey. Exp. Brain Res. 79:299–312 [Google Scholar]
  212. Vidal PP, May PJ, Baker R. 1988. Synaptic organization of the tectal-facial pathways in the cat. I. Synaptic potentials following collicular stimulation. J. Neurophysiol. 60:769–97 [Google Scholar]
  213. Vokoun CR, Huang X, Jackson MB, Basso MA. 2014. Response normalization in the superficial layers of the superior colliculus as a possible mechanism for saccadic averaging. J. Neurosci. 34:7976–87 [Google Scholar]
  214. Vokoun CR, Jackson MB, Basso MA. 2010. Intralaminar and interlaminar activity within the rodent superior colliculus visualized with voltage imaging. J. Neurosci. 30:10667–82 [Google Scholar]
  215. Wallace MT, Meredith MA, Stein BE. 1993. Converging influences from visual, auditory, and somatosensory cortices onto output neurons of the superior colliculus. J. Neurophysiol. 69:1797–809 [Google Scholar]
  216. Wang L, Liu M, Segraves MA, Cang J. 2015. Visual experience is required for the development of eye movement maps in the mouse superior colliculus. J. Neurosci. 35:12281–86 [Google Scholar]
  217. Wang S-R. 2003. The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Res. Rev. 41:13–25 [Google Scholar]
  218. Wang Y, Luksch H, Brecha NC, Karten HJ. 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 [Google Scholar]
  219. Watanabe M, Kobayashi Y, Inoue Y, Isa T. 2005. Effects of local nicotinic activation of the superior colliculus on saccades in monkeys. J. Neurophysiol. 93:519–34 [Google Scholar]
  220. Westby GW, Collinson C, Redgrave P, Dean P. 1994. Opposing excitatory and inhibitory influences from the cerebellum and basal ganglia converge on the superior colliculus: an electrophysiological investigation in the rat. Eur. J. Neurosci. 6:1335–42 [Google Scholar]
  221. White BJ, Boehnke SE, Marino RA, Itti L, Munoz DP. 2009. Color-related signals in the primate superior colliculus. J. Neurosci. 29:12159–66 [Google Scholar]
  222. Wickelgren BG. 1971. Superior colliculus: some receptive field properties of bimodally responsive cells. Science 173:69–72 [Google Scholar]
  223. Wise LZ, Irvine DR. 1983. Auditory response properties of neurons in deep layers of cat superior colliculus. J. Neurophysiol. 49:674–85 [Google Scholar]
  224. Wolf AB, Lintz MJ, Costabile JD, Thompson JA, Stubblefield EA, Felsen G. 2015. An integrative role for the superior colliculus in selecting targets for movements. J. Neurophysiol. 114:2118–31 [Google Scholar]
  225. Wolfe JM, Horowitz TS. 2004. What attributes guide the deployment of visual attention and how do they do it?. Nat. Rev. Neurosci. 5:495–501 [Google Scholar]
  226. Wurtz RH, Goldberg ME. 1972. Activity of superior colliculus in behaving monkey: III. Cells discharging before eye movements. J. Neurophysiol. 35:575–86 [Google Scholar]
  227. Zenon A, Krauzlis RJ. 2012. Attention deficits without cortical neuronal deficits. Nature 489:434–37 [Google Scholar]
/content/journals/10.1146/annurev-vision-102016-061234
Loading
/content/journals/10.1146/annurev-vision-102016-061234
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