Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense

Frontiers in Neuroanatomy

Volumn , Issue APRIL 2012, 2012, Pages

  Comoli, Eliane ^a   Favaro, Plínio Das Neves ^a   Vautrelle, Nicolas ^b   Leriche, Mariana ^b   Overton, Paul G ^b   Redgrave, Peter ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Approach; Defense; Segregated anatomical inputs; Superior colliculus

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTRANSFORMATION; BRAIN FUNCTION; BRAIN STEM; CELL DENSITY; CONDITIONING; CONTROLLED STUDY; DEFENSE MECHANISM; DIENCEPHALON; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; LATERAL GENICULATE BODY; LATERAL RETICULAR NUCLEUS; LOCUS CERULEUS; MALE; MICROSCOPY; NEUROANATOMY; NONHUMAN; PRIMARY SOMATOSENSORY CORTEX; RAT; SENSORIMOTOR FUNCTION; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS RETICULATA; SUPERIOR COLLICULUS; TECTUM; THALAMUS; TOPOGRAPHY; VISUAL FIELD; ZONA INCERTA;

EID: 84863888223     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2012.00009     Document Type: Article

References (122)

1. Alloway, K. D., Smith, J. B., and Beau-chemin, K. J. (2010). Quantitative analysis of the bilateral brainstem projections from the whisker and forepaw regions in rat primary motor cortex. J. Comp. Neurol. 518, 4546-4566.
2. Appell, P. P., and Behan, M. (1990). Sources of subcortical GABAergic projections to the superior collicu-lus in the cat. J. Comp. Neurol. 302, 143-158.
3. Arnault, P., and Roger, M. (1990). Ventral temporal cortex in the rat: connections of secondary auditory areas Te2 and Te3. J. Comp. Neurol. 302, 110-123.
4. Aronoff, R., Matyas, F., Mateo, C., Ciron, C., Schneider, B., and Petersen, C. C. H. (2010). Long-range connectivity of mouse primary somatosensory barrel cortex. Eur. J. Neurosci. 31, 2221-2233.
5. Bajo, V. M., Merchán, M. A., Malmierca, M. S., Nodal, F. R., and Bjaalie, J. G. (1999). Topographic organization of the dorsal nucleus of the lateral lemniscus in the cat. J. Comp. Neurol. 407, 349-366.
6. Balatoni, B., and Detari, L. (2003). EEG related neuronal activity in the pedunculopontine tegmental nucleus of urethane anaesthetized rats. Brain Res. 959, 304-311.
7. Bernard, J. F., and Besson, J. M. (1990). The spino(trigemino) pontoamygdaloid pathway: elec-trophysiological evidence for an involvement in pain processes. J. Neurophysiol. 63, 473-490.
8. Bernard, J. F., Huang, G. F., and Besson, J. M. (1994). The parabrachial area: electrophysiological evidence for an involvement in visceral nociceptive processes. J. Neurophysiol. 71, 1646-1660.
9. Bester, H., Menendez, L., Besson, J. M., and Bernard, J. F. (1995). Spino (trigemino) parabrachiohypothala-mic pathway: electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 73, 568-585.
10. Billington, J., Wilkie, R. M., Field, D. T., and Wann, J. P. (2011). Neural processing of imminent collision in humans. Proc. Biol. Sci. 278, 1476-1481.
11. Bon, K., Lantéri-Minet, M., de Pom-mery, J., Michiels, J. F., and Menétrey, D. (1996). Cyclophosphamide cystitis as a model of visceral pain in rats. A survey of hindbrain structures involved in visceroception and nociception using the expression of c-Fos and Krox-24 proteins. Exp. Brain Res. 108, 404-416.
12. Born, G., and Schmidt, M. (2008). Arec-iprocal connection between the ventral lateral geniculate nucleus and the pretectal nuclear complex and the superior colliculus: an in vitro characterization in the rat. Vis. Neu-rosci. 25, 39-51.
13. Brog, J. S., Salyapongse, A., Deutch, A. Y., and Zahm, D. S. (1993). The patterns of afferent innervation of the core and shell in the "accum-bens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J. Comp. Neurol. 338, 255-278.
14. Buchanan, S. L., Thompson, R. H., Maxwell, B. L., and Powell, D. A. (1994). Efferent connections of the medial prefrontal cortex in the rabbit. Exp. Brain Res. 100, 469-483.
15. Cadusseau, J., and Roger, M. (1985). Afferent projections to the superior colliculus in the rat, with special attention to the deep layers. J. Hirnforsch. 26, 667-681.
16. Canteras, N. S., and Goto, M. (1999). Connections of the precommissural nucleus. J. Comp. Neurol. 408, 23-45.
17. Canteras, N. S., Simerly, R. B., and Swanson, L.W. (1994). Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin studyintherat. J. Comp. Neurol. 348, 41-79.
18. Canteras, N. S., and Swanson, L. W. (1992). The dorsal premammillary nucleus: an unusual component of the mammillary body. Proc. Natl. Acad. Sci. U.S.A. 89, 10089-10093.
19. Carlson, J. D., Iacono, R. P., and Maeda, G. (2004). Nociceptive excited and inhibited neurons within the pedun-culopontine tegmental nucleus and cuneiform nucleus. Brain Res. 1013, 182-187.
20. Carvalho-Netto, E. F., Markham, C., Blanchard, D. C., Nunes-de-Souza, R. L., and Blanchard, R. J. (2006). Physical environment modulates the behavioral responses induced by chemical stimulation of dorsal periaqueductal gray in mice. Pharmacol. Biochem. Behav. 85, 140-147.
21. Chubb, M. C., and Fuchs, A. F. (1982). Contribution of y group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements. J. Neurophysiol. 48, 75-99.
22. Coizet, V., Dommett, E. J., Redgrave, P., and Overton, P. G. (2006). Nociceptive responses of midbrain dopaminergic neurones are modulated by the superior colliculus in the rat. Neuroscience 139, 1479-1493.
23. Coizet, V., Graham, J. H., Moss, J., Bolam, J. P., Savasta, M., McHaffie, J. G., Redgrave, P., and Overton, P. G. (2007). Short-latencyvisual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J. Neurosci. 29, 5701-5709.
24. Comoli, E., Favaro, P. D. N., and Mercez, P. L. C. (2010). "Superior colliculus: an important neural site involved in motivated behaviors, " in Proceedings of the 40th Annual Meeting of the Society for Neuroscience, abstr. 813.17, San Diego, CA.
25. Cornwall, J., Cooper, J. D., and Phillip-son, O. T. (1990). Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat. Brain Res. Bull. 25, 271-284.
26. Corvisier, J., and Hardy, O. (1993). Distribution of synaptic terminals from prepositus neurones on the collicu-lar maps. Neuroreport 4, 511-514.
27. Dean, P., Redgrave, P., Sahibzada, N., and Tsuji, K. (1986). Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19, 367-380.
28. Dean, P., Redgrave, P., andWestby, G. W. M. (1989). Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12, 137-147.
29. Dillon, L. S. (1962). Comparative notes on the cerebellum of the monotremes. I. Contribution toward a phylogeny of the monotremes. I. Contribution toward a phylogeny of the mammalian brain. J. Comp. Neurol. 118, 343-353.
30. Druga, R., and Syka, J. (1984). Projections from auditory structures to the superior colliculus in the rat. Neurosci. Lett. 45, 247-252
31. Favaro, P. D. N., Gouvea, T. S., De Oliveira, S. R., Vautrelle, N., Redgrave, P., and Comoli, E. (2011). The influence of vibrissal somatosensory processing in rat superior colliculus on prey capture. Neuroscience 176, 318-327.
32. Ficalora, A. S., and Mize, R. R. (1989). The neurons of the substantia nigra and zona incerta which project to the superior col-liculus are GABA immunoreactive: a double-label study using GABA imunocytochemistry and lectin retrograde transport. Neuroscience 29, 567-581.
33. Furigo, I. C., De Oliveira, W. F., De Oliveira, A. R., Comoli, E., Baldo, M. V., Mota-Ortiz, S. R., and Canteras, N. S. (2010). The role of the superior colliculus in predatory hunting. Neuroscience 165, 1-15.
34. Gaither, N. S., and Stein, B. E. (1979). Reptiles and mammals use similar sensory organizations in the midbrain. Science 205, 595-597.
35. Garcia Del Caño, G., Gerrikagoitia, I., and Martínez-Millán, L. (2000). Morphology and topographical organization of the retrosplenio-collicular connection: a pathway to relay contextual information from the environment to the superior colliculus. J. Comp. Neurol. 425, 393-408.
36. Gauriau, C., and Bernard, J. F. (2002). Pain pathway and parabrachial circuits in the rat. Exp. Physiol. 87, 251-258.
37. Glickstein, M. (2003). Subcortical projections of the parietal lobes. Adv. Neurol. 93, 43-55.
38. Gruart, A., and Delgado-García, J. M. (1994). Signalling properties of identified deep cerebellar nuclear neurons related to eye and head movements in the alert cat. J. Physiol. 478(Pt 1), 37-54.
39. Harting, J. K., Updyke, B. V., and Van Lieshout, D. P. (1992). Corticotec-tal projections in the cat: anterograde transport studies of twenty-five cortical areas. J. Comp. Neurol. 324, 379-414.
40. Harvey, A. R., and Worthington, D. R. (1990). The projection from different visual cortical areas to the rat superior colliculus. J. Comp. Neurol. 298, 281-292.
41. Henkel, C. K., and Schneiderman, A. (1988). Nucleus sagulum: projections of a lateral tegmental area to the inferior colliculus in the cat. J. Comp. Neurol. 271, 577-588.
42. Hoffer, Z. S., Arantes, H. B., and Roth, R. L. Alloway, K. D. (2005). Functional circuits mediating sensorimotor integration: quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons. J. Comp. Neurol. 488, 82-100.
43. Huerta, M. F., Frankfurter, A., and Harting, J. K. (1983). Studies of the principal sensory and spinal trigeminal nuclei of the rat: projections to the superior colliculus, inferior olive, and cerebellum. J. Comp. Neurol. 220, 147-167.
44. Huerta, M. F., and Harting, J. K. (1982). The projection from the nucleus of the posterior commissure to the superior colliculus of the cat: patchlike endings within the intermediate and deep grey layers. Brain Res. 238, 426-432.
45. Hurley, K. M., Herbert, H., Moga, M. M., and Saper, C. B. (1991). Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 308, 249-276.
46. Itoh, K., Konishi, A., Nomura, S., Mizuno, N., Nakamura, Y., and Sugimoto, T. (1979). Application of coupled oxidation reaction to electron microscopic demonstration of horseradish peroxidase: cobalt-glucose oxidase method. Brain Res. 175, 341-346.
47. Kass, J. H. (1995). The evolution of isocortex. Brain Behav. Evol. 46, 187-196.
48. Kass, J. H. (2004). Evolution of somatosensory and motor cortex in primates. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 281A, 1148-1156.
49. Kass, J. H. (2011). Neocortex in early mammals and its subsequent variations. Ann. N. Y. Acad. Sci. 1225, 28-36.
50. Kawakura, S., Hattori, S., Higo, S., and Matsuyama, T. (1982). The cerebellar projections to the superior col-liculus and pretectum in the cat: an autoradiographic and horseradish study. Neuroscience 7, 1675-1689.
51. Kelly, J. B., Buckthought, A. D., and Kidd, S. A. (1998). Monaural and binaural response properties of single neurons in the rat's dorsal nucleus of the lateral lemniscus. Hear. Res. 122, 25-40.
52. Kelly, J. B., Van Del, B. A., and Ito, M. (2009). Anatomical projections of the nuclei of the lateral lemniscus in the albino aat (Rattus norvegicus). J. Comp. Neurol. 512, 573-593.
53. Killackey, H. P., and Erzurumlu, R. S. (1981). Trigeminal projections to the superior colliculus of the rat. J. Comp. Neurol. 201, 221-242.
54. Kimura, A., Donishi, T., Okamoto, K., and Tamai, Y. (2004). Efferent connections of posterodorsal auditory area in the rat cortex: implications for auditory spatial processing. Neuroscience 128, 399-419.
55. King, S. M., Shehab, S., Dean, P., and Redgrave, P. (1996). Differential expression of fos-like immunoreactivity in the descending projections of superior colliculus after electrical stimulation in the rat. Behav Brain Res. 78, 131-145.
56. Klooster, J., Vrensen, G. F. J. M., Miiller, L.J., and van der Want, J. J. L. (1995). Efferent projections of the olivary pretectal nucleus in the albino rat subserving the pupillary light reflex and related reflexes. A light microscopic tracing study. Brain Res. 688, 34-46.
57. Klop, E. M., Mouton, L. J., Ehling, T., and Holstege, G. (2005). Two parts of the nucleus hypoglossi project to two different subdivisions of the dorsolateral periaqueductal gray in cat. J. Comp. Neurol. 492, 303-322.
58. Kolmac, C. I., Power, B. D., and Mitro-fanis, J. (1998). Patterns of connections between zona incerta and brainstem in rats. J. Comp. Neurol. 396, 544-555.
59. Krauthamer, G. M., Grunwerg, B. S., and Krein, H. (1995). Putative cholinergic neurons of the pedunculopon-tine tegmental nucleus projecting to the superior colliculus consist of sensory responsive and unresponsive populations which are functionally distinct from other mesopontine neurons. Neuroscience 69, 507-517.
60. Lee, T., and Kim, U. (2012). Descending projections from the dysgranu-lar zone of rat primary somatosensory cortex processing deep somatic input. J. Comp. Neurol. 520, 10211046.
61. Leichnetz, G. R., and Gonzalo-Ruiz, A. (1987). Collateralization of frontal eye field (medial precentral/anterior cingulate) neurons projecting to the paraoculomotor region, superior colliculus, and medial pontine reticular formation in the rat: a fluorescent double-labeling study. Exp. Brain Res. 68, 355-364.
62. Li, Y. Q., Takada, M., Kaneko, T., and Mizuno, N. (1995). Premotor neurons for trigeminal motor nucleus neurons innervating the jaw-closing and jaw-opening muscles: differential distribution in the lower brainstem of the rat. J. Comp. Neurol. 356, 563-579.
63. Li, Y. Q., Takada, M., Kaneko, T., and Mizuno, N. (1996). GABAergic and glycinergic neurons projecting to the trigeminal motor nucleus: a double labeling study in the rat. J. Comp. Neurol. 373, 498-510.
64. Liu, Y. J., Wang, Q., and Li, B. (2011). Neuronal responses to looming objects in the superior collicu-lus of the cat. Brain Behav. Evol. 77, 193-205.
65. Lynch, J. C., Graybiel, A. M., and Lobeck, L. J. (1985). The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. J. Comp. Neurol. 235, 241-254.
66. Manger, P. R., Restrepo, C. E., and Innocenti, G. M. (2010). The superior colliculus of the ferret: cortical afferents and efferent connections to dorsal thalamus. Brain Res. 1353, 74-85.
67. May, P. J. (2006). The mammalian superior colliculus: laminar structure and connections. Prog. Brain Res. 151, 321-378.
68. May, P. J., Sun, W., and Hall, W. C. (1997). Reciprocal connections between the zona incerta and the pretectum and superior collicu-lus of the cat. Neuroscience 77, 1091-1114.
69. McIntyre, D. C., Kelly, M. E., and Staines, W. A. (1996). Efferent projections of the anterior perirhinal cortex in the rat. J. Comp. Neurol. 369, 302-318.
70. Menendez, L., Bester, H., Besson, J. M., and Bernard, J. F. (1996). Parabrachial area: electrophysiolog-ical evidence for an involvement in coldnociception. J. Neurophysiol. 75, 2099-2115.
71. Meredith, M. A., and Clemo, R. H. (1989). Auditory cortical projection from the anterior ectosylvian sulcus (field AES) to the superior colliculus in the cat: an anatomical andelectro-physiological study. J. Comp. Neurol. 289, 687-707.
72. Montagnini, A., and Treves, A. (2003). The evolution of mammalian cortex, from lamination to arealization. Brain Res. Bull. 60, 387-393.
73. Moore, R. Y., Weis, R., and Moga, M. M. (2000). Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J. Comp. Neurol. 420, 398-418.
74. Nagata, T., and Hayashi, Y. (1984). The visual field representation of the rat ventral lateral geniculate nucleus. J. Comp. Neurol. 227, 582-588.
75. Ndiaye, A., Pinganaud, G., Buisseret-Delmas, C., Buisseret, P., and Van-dewerf, F. (2002). Organization of trigeminocollicular connections and their relations to the sensory innervation of the eyelids in the rat. J. Comp. Neurol. 448, 373-387.
76. Nicolelis, M. A., Chapin, J. K., and Lin, R. C. (1992). Somatotopic maps within the zona incerta relay parallel GABAergic somatosensory pathways to the neocortex, superior col-liculus, and brainstem. Brain Res. 577, 134-141.
77. Ohtsuki, H., Tokunaga, A., Ono, K., Hasebe, S., and Tadokoro, Y. (1992). Distribution of efferent neurons projecting to the tectum and cerebellum in the rat prepositus hypoglossi nucleus. Invest. Ophthalmol. Vis. Sci. 33, 2567-2574.
78. Olucha-Bordonau, F. E., Tervel, V., Bracia-González, J., Ruiz-Torner, A., Valverde-Navarro, A. A., and Martínez-Soriano, F. (2003). Cytoar-chitecture and efferent projections of the nucleus incertus of the rat. J. Comp. Neurol. 464, 62-97.
79. Páli, J., Baldauf, Z. A., Szentpétery, Z., Szabó, Z., Herczeg, L., and Görcs, T. J. (2002). Chemoanatomical separation of vibrissal trigeminal primary afferents in the rat: a special central representation of supraorbital vibrissae. Somatosens. Mot. Res. 19, 245-254.
80. Paxinos, G., andWatson, C. (2007). The Rat Brain in Steretaxic Coordinates, 6th Edn. San Diego: Elsevier.
81. Pieribone, V. A., and Aston-Jones, G. (1988). The iontophoretic application of fluoro-gold for the study of afferents to deep brain nuclei. Brain Res. 475, 259-271.
82. Redgrave, P., Marrow, L., and Dean, P. (1992). Topographical organization of the nigrotectal projection in rat: evidence for segregated channels. Neuroscience 50, 571-595.
83. Redgrave, P., Prescott, T. J., and Gurney, K. (1999). The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89, 1009-1023.
84. Reep, R. L., Corwin, J. V., Hashimoto, A., and Watson, R. T. (1987). Efferent connections of the rostral portion of medial agranular cortex in rats. Brain. Res. Bull. 19, 203-221.
85. Rhoades, R. W., Fish, S. E., Chiaia, N. L., Bennett-Clarke, C., and Mooney, R. D. (1989). Organization of the projections from the trigeminal brainstem complex to the superior col-liculus in the rat and hamster: anterograde tracing with Phaseolus vulgaris leucoagglutinin and intra-axonal injection. J. Comp. Neurol. 289, 641-656.
86. Ricardo, J. A. (1981). Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Res. 214, 43-60.
87. Roldán, M., and Reinoso-Suárez, F. (1981). The cerebellar projections to the superior colliculus in the cat. J. Neurosci. 8, 827-834.
88. Room, P., Russchen, F. T., Groemewe-gen, H. J., and Lohman, A. H. M. (1985). Efferent connections of the prelimbic (area 32) and the infralim-bic (area25) cortices: an anterograde tracing study in the cat. J. Comp. Neurol. 242, 40-55.
89. Sahibzada, N., Dean, P., and Redgrave, P. (1986). Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J. Neurosci. 6, 723-733.
90. Saitoh, K., Ménard, A., and Griller, S. (2007). Tectal control of locomotion, steering, and eye movements in lamprey. J. Neurophysiol. 97, 3093-3108.
91. Satoh, K., and Fibiger, H. C. (1986). Cholinergic neurons of the lat-erodorsal tegmental nucleus: efferent and afferent connections. J. Comp. Neurol. 253, 277-302.
92. Scarnati, E., and Florio, T. (1997). The pedunculopontine nucleus and related structures. Functional organization. Adv. Neurol. 74, 97-110.
93. Schmued, L. C., andFallon, J. H. (1986). Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res. 377, 147-154.
94. Sefton, A. J., Dreher, B., and Harvey, A. (2004). "Visual system, " in The Rat Nervous System, 3rd Edn, ed. G. Paxinos (Amsterdam: Elsevier), 1082-1202.
95. Sesack, S. R., Deutch, A. Y., Roth, R. H., and Bunney, B. S. (1989). Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracingstudywith Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290, 213-242.
96. Shammah-Lagnado, S. J., Costa, M. S., and Ricardo, J. A. (1992). Afferent connections of the parvocel-lular reticular formation: a horseradish peroxidase study in the rat. Neuroscience 50, 403-425.
97. Shehab, S., Alzigali, L., Madathil, M., and Redgrave, P. (2007). Pharmacological evidence for an anticonvulsant relay in the rat ventromedial medulla. Eur. J. Neurosci. 26, 2585-2594.
98. Simpson, K., Wang, Y., and Lin, R. C. (2008). Patterns of convergence in rat zona incerta from the trigeminal nuclear complex: light and electron microscopic study. J. Comp. Neurol. 507, 1521-1541.
99. Sokov, A. Y., Lyubashina, O. A., and Panteleev, S. S. (2011). Spinal trigeminal neurons demonstrate an increase in responses to dural electrical stimulation in the orofacial formalin test. J. Headache Pain 13, 75-82.
100. Sparks, D. L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: role of the primate superior colliculus. Physiol. Rev. 66, 118-171.
101. Stein, B. E. (1981). Organization of the rodent superior colliculus: some comparisons with other mammals. Behav. Brain Res. 3, 175-188.
102. Stein, B. E. (1984). Development of the superior colliculus. Annu. Rev. Neurosci. 7, 95-125.
103. Stein, B. E., and Meredith, M. A. (1993). The Merging of the Senses. Cambridge, MA: The MIT Press.
104. Stephenson-Jones, M., Samuelsson, E., Ericsson, J., Brita, R., and Grillner, S. (2011). Evolutionaryconservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr. Biol. 21, 1081-1091.
105. Swanson, L. W. (2004). Brain Maps III: Structure of the Rat Brain. London: Elsevier.
106. Swanson, L. W., Cowan, W. M., and Jones, E. G. (1974). An autoradiographic study of the efferent connections of in the ventral lateral geniculate nucleus the albino rat and the cat. J. Comp. Neurol. 156, 143-163.
107. Takahashi, L. K., Chan, M. M., Mark, L., and Pilar, M. L. (2008). Predator odor fear conditioning: current perspectives and new directions. Neu-rosci. Biobehav. Rev. 32, 1218-1227.
108. Tanaka, K., Otani, K., Tokunaga, A., and Sugita, S. (1985). The reciprocal connections of the supra-geniculate nucleus and the superior colliculus in the rat. Neurosci. Res. 3, 79-85.
109. Telford, S., Wang, S., and Redgrave, P. (1986). Analysis of nociceptive neurones in the rat superior colliculus using c-fos immunohistochemistry. J. Comp. Neurol. 375, 601-617.
110. Trejo, L. J., and Cicerone, C. M. (1984). Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Res. 300, 49-62.
111. Updyke, B.V.(1977). Topographicorga-nization of the projections from cortical areas 17, 18, and 19 onto the thalamus, pretectum and superior colliculus in the cat. J. Comp. Neurol. 173, 81-122.
112. Van Groen, T., and Wyss, J. M. (1992). Connections of the retrosplenial dysgranular cortex in the rat. J. Comp. Neurol. 315, 200-216.
113. Vaudano, E., Legg, C. R., and Glick-stein, M. (1991). Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur. J. Neurosci. 3, 317-330.
114. Vertes, R. P., and Martin, G. F. (1988). Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J. Comp. Neurol. 275, 11-41.
115. Vertes, R. P., Martin, G. F., and Waltzer, R. (1986). An autoradi ographic analysis of ascending pro-jectionsfromthemedullaryreticular formation in the rat. Neuroscience 19, 873-398.
116. Wang, S., and Redgrave, P. (1997). Microinjections of muscimol into lateral superior colliculus disrupt orienting and oral movements in the formalin model of pain. Neuroscience 81, 967-988.
117. Waterhouse, B. D., Border, B., Wahl, L., and Mihailoff, G. A. (1993). Topographic organization of rat locus coeruleus and dorsal raphe nuclei: distribution of cells projecting to visual system structures. J. Comp. Neurol. 336, 345-361.
118. Westby, G. W., Keay, K. A., Redgrave, P., Dean, P., and Bannister, M. (1990). Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties. Exp. Brain Res. 81, 626-638.
119. Wiberg, M. (1992). Reciprocal connections between the periaqueductal gray matter and other somatosensory regions of the cat midbrain: a possible mechanism of pain inhibition. Ups. J. Med. Sci. 97, 37-47.
120. Wise, S. P., and Jones, E. G. (1977). Somatotopic and columnar organization in the corticotectal projection of the rat somatic sensory cortex. Brain Res. 133, 223-235.
121. Wurtz, R. H., and Albano, J. E. (1980). Visual-motor function of the primate superior colliculus. Annu. Rev. Neurosci. 3, 189-226.
122. Wyss, J. M., and Sripanidkulchai, K. (2003). The topography of the mesencephalic and pontine projections from the cingulate cortex of the rat. Brain Res. 293, 1-15.