Honeycomb-like structure of the intermediate layers of the rat superior colliculus, with additional observations in several other mammals: AChE patterning

Journal of Comparative Neurology

Volumn 419, Issue 2, 2000, Pages 137-153

  Chevalier, Gilles ^a   Mana, S ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Acetylcholinesterase; Cat; Hamster; Monkey; Mouse; Tectum

Indexed keywords

ACETYLCHOLINESTERASE;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CAT; ENZYME ACTIVITY; ENZYME LOCALIZATION; MALE; MONKEY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; STEREOMETRY; SUPERIOR COLLICULUS; SYRIAN HAMSTER;

EID: 0034011478     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000403)419:2<137::AID-CNE1>3.0.CO;2-6     Document Type: Article

References (129)

1. Asanuma H, Rosen I. 1972. Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp Brain Res 14:243-256.
2. Beckstead RM, Domesick VB, Nauta WJH. 1979. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191-217.
3. Behan M, Appell PP. 1992. Intrinsic circuitry in the cat superior colliculus: projections from the superficial layers. J Comp Neurol 315:230-243.
4. Behan M, Appell PP, Kime N. 1995. Postnatal development of substance P immunoreactivity in the rat superior colliculus. Vis Neurosci 10:1121-1127.
5. Beninato M, Spencer RF. 1986. Cholinergic projections to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. J Comp Neurol 253: 525-538.
6. Caldwell RB, Mize RR. 1981. Superior colliculus neurons that project to the cat lateral posterior nucleus have varying morphologies. J Comp Neurol 203:43-66.
7. Casagrande VA, Harting JK, Hall WC, Diamond IT, Martin GF. 1972. Superior colliculus of the tree shrew (Tupaia glis): evidence for a structural and functional subdivision into superficial and deep layers. Science 177:444-447.
8. Castiglioni AJ, Gallaway MC, Coulter JD. 1978. Spinal projection from the midbrain in the monkey. J Comp Neurol 178:329-345.
9. Chalupa LM, Rhoades R.W. 1977. Responses of visual, somatosensory and auditory neurons in the golden hamster's superior colliculus. J Physiol 270:595-626.
10. Chalupa LM, Rhoades RW. 1979 An autoradiographic study of the retinotectal projection in the golden hamster. J Comp Neurol 186:561-570.
11. Chevalier G, Deniau JM. 1984. Spatiotemporal organization of a branched tecto-spinal/tecto-diencephalic neuronal system. Neuroscience 12:427-439.
12. Chevalier G, Vacher S, Deniau JM. 1984. Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behavior. Exp Brain Res 53:320-326.
13. Clemo HR, Stein BE. 1983. Organization of a fourth somatosensory area in cat. J Neurophysiol 50:910-925.
14. Cowie RJ, Robinson DL. 1994. Subcortical contributions to head movements in macaques. I. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus. J Neurophysiol 72:2648-2664.
15. Cowie RJ, Smith MK, Robinson DL. 1994. Subcortical contributions to head movements in macaques. II. Connections of a medial pontomedullary head movement region. J Neurophysiol 72:2665-2682.
16. Dean P, Redgrave P, Westby GWM. 1989. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137-147.
17. Donaldson IML, Long AC. 1980. Interactions between extraocular proprioceptive and visual signals in the superior colliculus of the cat. J Physiol (Lond) 298:85-110.
18. Dräger U, Hubel DH. 1975. Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. J Neurophysiol 38:690-713.
19. Edwards SB. 1980. The deep layers of the superior colliculus: their reticular characteristics and structural organization. In: Hobson JA, Brazier MAB, editors. The reticular formation revisited. New York: Raven Press. p 193-209.
20. Edwards SB, Ginsburg CL, Henkel CK, Stein BE. 1979. Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184:309-330.
21. Feldon S, Feldon P, Kruger L. 1970. Topography of the retinal projection upon the superior colliculus of the cat. Vision Res 10:135-143.
22. Finlay BL, Schneps SE, Wilson KG, Schneider G. 1978. Topography of visual and somatosensory projections to the superior colliculus of the golden hamster. Brain Res 142:223-235.
23. Geneser-Jensen FA, Blackstad JW. 1971. Distribution of acetylcholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, para subiculum and presubiculum. Z Zellforsch Mikrosk Anat 114: 460-481.
24. Goldberg ME, Wurtz RH. 1972. Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. J Neurophysiol 35:542-559.
25. Goldman PS, Nauta WJH. 1976. Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey. Brain Res 116:145-149.
26. Gordon BG. 1973. Receptive fields in the deep layers of the cat superior colliculus. J Neurophysiol 36:157-178.
27. Graham J. 1982. Some topographical connections of the striate cortex with subcortical structures in macaca fascicularis. Exp Brain Res 47:1-14.
28. Grantyn R. 1988. Gaze control through superior colliculus: structure and function. In: Büttner-Ennever JA, editor. The neuroanatomy of the oculomotor system. Reviews of oculomotor research. Amsterdam: Elsevier Science. p 273-333.
29. Grantyn A, Grantyn R. 1982. Axonal patterns and sites of termination of cat superior colliculus neurons projecting to the tecto-bulbo-spinal tract. Exp Brain Res 46:243-256.
30. Grantyn R, Ludwig R, Eberhardt W. 1984. Neurons of the superficial tectal gray. An intracellular HRP study on the kitten superior colliculus in vitro. Exp Brain Res 55:172-176.
31. Graybiel AM. 1972. A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial layers of the superior colliculus. Brain Res 145:365-374.
32. Graybiel AM. 1975. Anatomical organization of retinotectal afferents in the cat: an autoradiographic study. Brain Res 96:1-23.
33. Graybiel AM. 1978a. Organization of the nigrotectal connection: an experimental tracer study in the cat. Brain Res 143:339-348.
34. Graybiel AM. 1978b. A stereometric pattern of distribution of acetylcholinesterase in deep layers of the superior colliculus. Nature 272:539-541.
35. Graybiel AM. 1979. Periodic compartmental distribution of acetylcholinesterase in the superior colliculus of the human brain. Neuroscience 4:643-650.
36. Graybiel AM, Illing RB. 1994. Enkephalin-positive and acetylcholinesterase-positive patch systems in the superior colliculus have matching distributions but distinct developmental histories. J Comp Neurol 340:297-310.
37. Graybiel AM, Brecha N, Karten HJ. 1984. Cluster-and-sheet pattern of enkephalin-like immunoreactivity in the superior colliculus of the cat. Neuroscience 12:191-214.
38. Hall WC, Fitzpatrick D, Klatt LL, Raczkowski D. 1989. Cholinergic innervation of the superior colliculus in the cat. J Comp Neurol 287:495-514.
39. Hallanger AE, Wainer BH. 1988. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J Comp Neurol 274: 483-515.
40. Harris LR. 1980. The superior colliculus and movements of the head and eyes in cats. J Physiol 300:367-391.
41. Harris LR, Blakemore C, Donaghy M. 1980. Integration of visual and auditory space in the mammalian superior colliculus. Nature 288:56-59.
42. Harting JK. 1977. Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta) J Comp Neurol 173:583-612.
43. Harting JK, Van Lieshout DP. 1991. Spatial relationships of axons arising from the substantia nigra, spinal trigeminal nucleus, and pedunculopontine tegmental nucleus, within the intermediate gray of the cat superior colliculus. J Comp Neurol 305:543-558.
44. Harting JK, Huerta MF, Frankfurter AJ, Strominger NL, Royce GJ. 1980. Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. J Comp Neurol 192: 853-882.
45. Hashikawa T. 1989. Regional and laminar distribution of choline acetyltransferase immunoreactivity in the cat superior colliculus. Neurosci Res 6:426-437.
46. Henderson Z, Sherriff FE. 1991. Distribution of choline acetyltransferase immunoreactive axons and terminals in the rat and ferret brainstem. J Comp Neurol 314:147-163.
47. Hilbig H, Schierwagen A. 1994. Interlayer neurons in the rat superior colliculus: a tracer study using DIL/Di-ASP. Neuroreport 12:477-480.
48. Holcombe V, Hall WC. 1981. Laminar origin of ipsilateral tecto-pontine pathways. Neuroscience 6:255-260.
49. Holstedge G, Collewijn H. 1982. The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. J Comp Neurol 209:139-175.
50. Hubel DH, Wiesel TN. 1977. Ferrier Lecture: functional architecture of macaque monkey visual cortex. Proc R Soc Lond (Biol) 198:1-59.
51. Hubel DH, Le Vay S, Wiesel TN. 1975. Mode of termination of retinotectal fibers in macaque monkey: an autoradiographic study. Brain Res 96: 25-40.
52. Huerta MF, Harting JK. 1982. The projection from the nucleus of the posterior commissure to the superior colliculus of the cat: patch-like endings within the intermediate and deep grey layers. Brain Res 238: 426-432.
53. Huerta MF, Harting JK. 1983. Sublamination within the superficial gray layer of the squirrel monkey: an analysis of the tecto-pulvinar projection using anterograde and retrograde methods. Brain Res 261:119-126.
54. Huerta MF, Harting JK. 1984. The mammalian superior colliculus: studies of its morphology and connections. In: Vanegas H, editor. Comparative neurology of the optic tectum. New York: Plenum. p 687-773.
55. Huerta MF, Frankfurter AJ, Harting JK. 1981. The trigeminocollicular projection in the cat: patch-like endings within the intermediate gray. Brain Res 211:1-13.
56. Illing RB. 1988. Spatial relation of the acetylcholinesterase rich domain to the visual topography in the feline superior colliculus. Exp Brain Res 73:589-594.
57. Illing RB. 1990. Choline acetyltransferase-like immunoreactivity in the superior colliculus of the cat and its relation to the pattern of acetylcholinesterase staining. J Comp Neurol 296:32-46.
58. Illing RB. 1996. The mosaic architecture of the superior colliculus. In: Norita M, Bando T, Stein B, editors. Extrageniculostriate mechanisms underlying visually guided orientation behavior. Progress in Brain Research 112:17-34.
59. Illing RB, Graybiel AM. 1985. Convergence of afferents from frontal cortex and substantia nigra onto acetylcholinesterase-rich patches in the cat's superior colliculus. Neuroscience 14:455-482.
60. Illing RB, Graybiel AM. 1986. Complementary and non-matching afferent compartments in the cat superior colliculus: innervation of the acetylcholinesterase-poor-domain of the intermediate gray layers. Neuroscience 18:373-394.
61. Illing RB, Wogt DM, Spatz WB. 1990. Parvalbumin in rat superior colliculus. Neurosci Lett 120:197-200.
62. Jayaraman A, Batton RR, Carpenter MB. 1977. Nigrotectal projection in the monkey: an autoradiographic study. Brain Res 135:147-152.
63. Jeon CJ, Mize RR. 1993. Choline acetyltransferase-immunoreactive patches overlaps specific efferent cell groups in the cat superior colliculus. J Comp Neurol 337:127-150.
64. Jones BE, Webster HH. 1988. Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. I. Effects upon the cholinergic innervation of the brain. Brain Res 451:13-32.
65. Kaas JH, Nelson RJ, Sur M, Merzenich MM. 1981. Organization of somatosensory cortex in primates. In: Schmitt FO, Worden FG, Adelman G, Dennis SG, editors. The organization of cerebral cortex: Proceedings of a Neurosciences Research Program Colloquium. Cambridge: MIT Press. p 237-261.
66. Kanaseki T, Sprague JM. 1974. Anatomical organization of pretectal nuclei and tectal laminae in the cat. J Comp Neurol 158:319-338.
67. Kawamura S, Hattori S, Higo S, Matsuyama T. 1982. The cerebellar projection to the superior colliculus and pretectum in the cat: an autoradiographic and horseradish peroxidase study. Neuroscience 7:1673-1689.
68. Kudo M. 1981. Projections of the nuclei of the lateral lemniscus in the cat: an autoradiographic study. Brain Res 221:57-69.
69. Kudo M, Niimi K. 1980. Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J Comp Neurol 191:545-556.
70. Künzle H, Akert K. 1977. Efferent connection of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J Comp Neurol 173:147-164.
71. Leichnetz GR, Spencer RF, Hardy SGP, Astruc J. 1981. The prefrontal corticotectal projection in the monkey: an anterograde and retrograde peroxidase study. Neuroscience 6:1023-1041.
72. McHaffie JG, Stein BE. 1982. Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247: 243-253.
73. McHaffie JG, Kao CK, Stein BE. 1989. Nociceptive neurons in rat superior colliculus: response properties, topography, and functional implications. J Neurophysiol 62:510-525.
74. Meredith MA, Stein BE. 1986. Visual, auditory and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol 56:640-662.
75. Miguel-Hidalgo JJ, Senba E, Matsuani S, Takatsuji K, Fukuji H, Tohyama M. 1989. Laminar and segregated distribution of immunoreactivities for some neuropeptides and adenosine deaminase in the superior colliculus of the rat. J Comp Neurol 280:410-423.
76. Mize RR. 1983. Patterns of convergence and divergence of retinal and cortical synaptic terminals in the cat superior colliculus. Brain Res 51:88-96.
77. Mize RR. 1989. Enkephalin-like immunoreactivity in the cat superior colliculus: distribution, ultrastructure and colocalization with GABA. J Comp Neurol 285:133-155.
78. Mooney RD, Nikoletseas MM, Hess PR, Allen L, Lewin AC, Rhoades RW. 1988. The projection from the superficial to the deep layers of the superior colliculus: an intracellular horseradish peroxidase injection in the hamster. J Neurosci 8:1384-1399.
79. Moschovakis AK, Karabelas AB. 1985. Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deep layers of the superior colliculus of the cat. J Comp Neurol 239:276-308.
80. Moschovakis AK, Karabelas AB, Highstein SM. 1988. Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. J Neurophysiol 60:232-262.
81. Munoz DP, Guitton D. 1991. Control of orienting gaze shifts by the tectoreticulospinal systems in the head-free cat. II. Sustained discharges during motor preparation and fixation. J Neurophysiol 66:1624-1641.
82. Munoz DP, Wurtz RH. 1993. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70: 559-575.
83. Murray EA, Coulter JD. 1982. Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Res 243:201-214.
84. Muto N, Kakei S, Shinoda Y. 1996, Morphology of single axons of tectospinal neurons in the upper cervical spinal cord. J Comp Neurol 372:9-26.
85. Northmore DPM, Levine ES, Schneider GE. 1988. Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595-605.
86. Paxinos G, Watson C. 1982. The rat brain in stereotaxic coordinates. London: Academic Press.
87. Paré M, Crommelinck M, Guitton D. 1994. Gaze shifts evoked by stimulation of the superior colliculus in the head-free cat conform to the motor map but also depend on stimulus strength and fixation activity. Exp Brain Res 101:123-139.
88. Ramon -Moliner E. 1972. Acetykholinesterase distribution in the brain-stem of the cat. Ergebn Anat Entwgesch 46:1-53.
89. Redgrave P, Odekunle A, Dean P. 1986. Tectal cells of origin of predorsal bundle in rat: location and segregation from ipsilateral descending pathway. Exp Brain Res 63:279-293.
90. Redgrave P, Marrow L, Dean P. 1992. Topographical organization of the nigrotectal projection in the rat: evidence for segregated channels. Neuroscience 50:571-595.
91. Redgrave P, McHaffie JG, Stein BE. 1996. Nociceptive neurons in rat superior colliculus. I. Antidromic activation from the contralateral predorsal bundle. Exp Brain Res 109:185-196.
92. Rhoades RW, Della Croce DR. 1980. Cells of origin of the tecto-spinal tract in the golden hamster: an anatomical and electrophysiological investigation. Exp Neurol 67:163-180.
93. Rhoades RW, Mooney RD, Klein BG, Jacquin MF, Szcepanik AM, Chiaia NL. 1987. The structural and functional characteristics of tectospinal neurons in the golden hamster. J Comp Neurol 255:451-465.
94. 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.
95. Rieck RW, Huerta MF, Harting JK, Weber JT. 1986. Hypothalamic and ventral thalamic projections to the superior colliculus in the cat. J Comp Neurol 243:249-265.
96. Robinson DA. 1972. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795-1808.
97. Ross CD, Godfrey DA. 1985. Distribution of choline acetyltransferase and acetylcholinesterase activities in layers of rat superior colliculus. J Histochem Cytochem 33:631-641.
98. Roucoux A, Crommelinck M. 1976. Eye movements evoked by superior colliculus stimulation in the alert cat. Brain Res 106:349-363.
99. Roucoux A, Guitton D, Crommelinck M. 1980. Stimulation of the superior colliculus in the alert cat. II. Eye and head movement evoked when the head is unrestrained. Exp Brain Res 39:75-85.
100. Sandell JH. 1984. The distribution of hexokinase compared with cytochrome oxidase and aceylcholinesterase in the somatosensory cortex and the superior colliculus of the rat. Brain Res 290:384-389.
101. Schiller PH, Koerner F. 1971. Discharge characteristics of single units in superior colliculus of the alert Rhesus monkey. J Neurophysiol 34:920-936.
102. Schiller PH, Stryker M. 1972. Single units recording and stimulation in superior colliculus of the alert Rhesus monkey. J Neurophysiol 35:915-924.
103. Segal RL, Beckstead RM, Kersey K, Edwards SB. 1983. The prefrontal corticotectal projection in the cat. Exp Brain Res 51:423-432.
104. Spangler KM, Morley BJ. 1987. Somatostatin-like immunochemistry in the midbrain of the cat. J Comp Neurol 260:87-97.
105. Sparks DL. 1988. Neural cartography: sensory and motor maps in the superior colliculus. Brain Behav Evol 31:49-56.
106. Sparks DL, Hartwich-Young R. 1989. The deep layers of the superior collieulus. In: Wurtz RH, Goldberg ME, editors. The neurobiology of saccadic eye movements. Reviews of oculomotor research. Vol 13. Amsterdam: Elsevier Science Publishers BV. p 213-255.
107. Sparks DL, Holland R, Guthrie BL. 1976. Size and distribution of movement fields in the monkey superior colliculus. Brain Res 113:21-34.
108. Stein BE. 1998. Neural mechanisms for synthetizing sensory information and producing adaptative behaviors. Exp Brain Res 123: 124-135.
109. Stein BE, Meredith MA. 1991. Functional organization of the superior colliculus. In: Leventhal AG, editor. The neural basis of visual function. Hampshire, UK: Macmillan Press. p 85-110.
110. Stein BE, Goldberg SJ, Clamann HP. 1976a. The control of eye movements by the superior colliculus in the alert cat. Brain Res 118:469-474.
111. Stein BE, Magalhaes-Castro B, Kruger L. 1976b. Relationship between visual and tactile representations in cat superior colliculus. J Neurophysiol 39:401-419.
112. Stryker MP, Schiller PH. 1975. Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp Brain Res 23:103-112.
113. Sugita S, Otani K, Tokunaga A, Terasawa K. 1983. Laminar origin of the tecto-thalamic projections in the albino rat. Neurosci Lett 43:143-147.
114. Swanson LW, Cowan WM, Jones EG. 1974. An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J Comp Neurol 156:143-164.
115. Syka J, Radil-Weiss T. 1971. Electrical stimulation of the tectum in freely moving cats. Brain Res 28:567-572.
116. Tashiro T, Kudo M, Kawamura S. 1980. Discontinuous spatial distribution of the tectal afferents from the trigeminal nucleus in the cat. Neurosci Lett 20:249-252.
117. Tiao YC, Blakemore C. 1976. Functional organization in the superior colliculus of the golden hamster. J Comp Neurol 168:483-504.
118. Toga AW, Santori EM. 1995. 3D spatial relationships of histochemical activity in the rat superior colliculus. Eur J Morphol 33:71-79.
119. Tokunaga A, Otani J. 1976. Dendritic patterns of neurons in the rat superior colliculus. Exp Neurol 52: 189-205.
120. Viktorov FV. 1968. Neuronal structure of corpora quadrigemina in the cat. Arkh Anat Gistol Embriol 54:45-55.
121. Wallace MN. 1986. Spatial relationship of histochemically demonstrable patches in the mouse superior colliculus. Exp Brain Res 62:241-249.
122. Wallace MN, Fredens K. 1988. Origin of high acetylcholinesterase activity in the mouse superior colliculus. Exp Brain Res 72:335-346.
123. Westby GWM, Keay KA, Redgrave P, Dean P, Bannister M. 1990. Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties. Exp Brain Res 81:626-638.
124. Wiener SI. 1986. Laminar distribution and patchiness of cytochrome oxidase in mouse superior colliculus. J Comp Neurol 244:137-148.
125. Wiener SI, Hartline PH. 1987. Perioral somatosensory but not visual inputs to the flank of the mouse superior colliculus. Neuroscience 21:557-564.
126. Woolf NJ, Butcher LL. 1986. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia and basal forebrain. Brain Res Bull 16:603-637.
127. Woolsey TA, Van der Loos H. 1970. The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex: description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242.
128. Wurtz RH, Goldberg ME. 1972. Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. J Neurophysiol 35:575-586.
129. Yamasaki DS, Krauthamer GM, Rhoades RW. 1986. Superior colliculus projection to intralaminar thalamus in rat: cells of origin. Brain Res 378:223-233.