Retinofugal projections in the mouse

Journal of Comparative Neurology

Volumn 522, Issue 16, 2014, Pages 3733-3753

  Lawrence, P Morin ^a   Studholme, Keith M ^a  

^a STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Auditory; Melanopsin; Nonimage forming; Olfactory; Retinorecipient; Subcortical; Visual system

Indexed keywords

CHOLERA TOXIN B SUBUNIT; DIAMINOBENZIDINE; CHOLERA TOXIN; MELANOPSIN; SCOTOPSIN;

ACCESSORY OPTIC TRACT SUPERIOR FASCICULUS; ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; BRAIN REGION; CONTROLLED STUDY; FOREBRAIN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; INNERVATION; MALE; MEDIAL TERMINAL NUCLEUS; MOUSE; NONHUMAN; PARANIGRAL NUCLEUS; PRETECTUM; PRIORITY JOURNAL; RETINA; RETINOFUGAL PROJECTION; SUPERIOR COLLICULUS; THALAMUS; THALAMUS NUCLEUS; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; HEMISPHERIC DOMINANCE; METABOLISM; PHYSIOLOGY; RETINA GANGLION CELL; THALAMUS INTRALAMINAR NUCLEUS; VISUAL SYSTEM;

ANIMALS; BRAIN MAPPING; CHOLERA TOXIN; FUNCTIONAL LATERALITY; INTRALAMINAR THALAMIC NUCLEI; MICE; MICE, INBRED C57BL; RETINA; RETINAL GANGLION CELLS; ROD OPSINS; VISUAL PATHWAYS;

EID: 84906790993     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23635     Document Type: Article

References (79)

1. Allen AE, Brown TM, Lucas RJ. 2011. A distinct contribution of short-wavelength-sensitive cones to light-evoked activity in the mouse pretectal olivary nucleus. J Neurosci 31:16833-16843.
2. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
3. 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.
4. Budinger E, Heil P, Scheich H. 2000. Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur J Neurosci 12:2452-2474.
5. Chen SK, Badea TC, Hattar S. 2011. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 476:92.
6. Clancy AN, Goldman BD, Bartke A, Macrides F. 1986. Reproductive effects of olfactory bulbectomy in the syrian-hamster. Biol Reprod 35:1202-1209.
7. Cooper AM, Cowey A. 1990. Development and retraction of a crossed retinal projection to the inferior colliculus in neonatal pigmented rats. Neuroscience 35:335-344.
8. Cooper HM, Herbin M, Nevo E. 1993. Visual system of a naturally microphthalmic mammal: The blind mole rat, Spalax ehrenbergi J Comp Neurol 328:313-350.
9. Cooper HM, Parvopassu F, Herbin M, Magnin M. 1994. Neuroanatomical pathways linking vision and olfaction in mammals. Psychoneuroendocrinology 19:623-639.
10. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin PD. 2005. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749-754.
11. Dhande OS, Huberman AD. 2014. Retinal ganglion cell maps in the brain: implications for visual processing. Curr Opin Neurobiol 24:133-142.
12. Dhande OS, Estevez ME, Quattrochi LE, El-Danaf RN, Nguyen PL, Berson DM, Huberman AD. 2013. Genetic dissection of retinal inputs to brainstem nuclei controlling image stabilization. J Neurosci 33:17797-17813.
13. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S. 2010. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:49-60.
14. Gaillard F, Karten HJ, Sauve Y. 2013. Retinorecipient areas in the diurnal murine rodent Arvicanthis niloticus: a disproportionally large superior colliculus. J Comp Neurol 521:1699-1726.
15. Giolli RA, Blanks RHI, Lui F. 2006. The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function. Neuroanat Oculomotor Sys 151:407-440.
16. Gooley JJ, Ho Mien I, St Hilaire MA, Yeo SC, Chua EC, van Reen E, Hanley CJ, Hull JT, Czeisler CA, Lockley SW. 2012. Melanopsin and rod-cone photoreceptors play different roles in mediating pupillary light responses during exposure to continuous light in humans. J Neurosci 32:14242-14253.
17. Goz D, Studholme K, Lappi DA, Rollag MD, Provencio I, Morin LP. 2008. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLoS One 3:e3153.
18. Guilding C, Hughes ATL, Piggins HD. 2010. Circadian oscillators in the epithalamus. Neuroscience 169:1630-1639.
19. Guler AD, Ecker JL, Lall GS, Haq S, Altimus CM, Liao HW, Barnard AR, Cahill H, Badea TC, Zhao H, Hankins MW, Berson DM, Lucas RJ, Yau KW, Hattar S. 2008. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453:102-105.
20. Harrington ME. 1997. The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci Biobehav Rev 21:705-727.
21. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N, Schmedt C, Jegla T, Panda S. 2008. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS One 3:e2451.
22. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. 2002. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065-1070.
23. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, Yau KW. 2003. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:76-81.
24. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497:326-349.
25. Horowitz SS, Blanchard JH, Morin LP. 2004. Intergeniculate leaflet and ventral lateral geniculate nucleus afferent connections: an anatomical substrate for functional input from the vestibulo-visuomotor system. J Comp Neurol 474:227-245.
26. Johnson RF, Moore RY, Morin LP. 1988. Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract. Brain Res 460:297-313.
27. Kagan R, Kainz V, Burstein R, Noseda R. 2013. Hypothalamic and basal ganglia projections to the posterior thalamus: possible role in modulation of migraine headache and photophobia. Neuroscience 248c:359-368.
28. Krauzlis RJ, Lovejoy LP, Zenon A. 2013. Superior colliculus and visual spatial attention. Annu Rev Neurosci 36:165-182.
29. Lee CC, Winer JA. 2008. Connections of cat auditory cortex: I. Thalamocortical system. J Comp Neurol 507:1879-1900.
30. Li X, Gilbert J, Davis FC. 2005. Disruption of masking by hypothalamic lesions in Syrian hamsters. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:23-30.
31. Ling C, Schneider GE, Jhaveri S. 1998. Target-specific morphology of retinal axon arbors in the adult hamster. Vis Neurosci 15:559-579.
32. Major DE, Rodman HR, Libedinsky C, Karten HJ. 2003. Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): anterograde tracing study using cholera toxin. J Comp Neurol 463:317-340.
33. Matteau I, Boire D, Ptito M. 2003. Retinal projections in the cat: a cholera toxin B subunit study. Vis Neurosci 20:481-493.
34. May PJ. 2006. The mammalian superior colliculus: laminar structure and connnections. Prog Brain Res 151:321-378.
35. Mikkelsen JD. 1992. Visualization of efferent retinal projections by immunohistochemical identification of cholera toxin subunit B. Brain Res Bull 28:619-623.
36. Mooney RD, Fish SE, Rhoades RW. 1984. Anatomical and functional organization of pathway from superior colliculus to lateral posterior nucleus in hamster. J Neurophysiol 51:407-431.
37. Morin LP. 1994. The circadian visual system. Brain Res Rev 67:102-127.
38. Morin LP. 2013a. Neuroanatomy of the extended circadian rhythm system. Exp Neurol 243:4-20.
39. Morin LP. 2013b. Nocturnal light and nocturnal rodents: similar regulation of disparate functions? J Biol Rhythms 28:95-106.
40. Morin LP, Allen CN. 2006. The circadian visual system, 2005. Brain Res Rev 51:1-60.
41. Morin LP, Blanchard JH. 1997. Neuropeptide Y and enkephalin immunoreactivity in retinorecipient nuclei of the hamster pretectum and thalamus. Vis Neurosci 14:765-777.
42. Morin LP, Blanchard JH. 1998. Interconnections among nuclei of the subcortical visual shell: the intergeniculate leaflet is a major constituent of the hamster subcortical visual system. J Comp Neurol 396:288-309.
43. Morin LP, Blanchard JH. 1999. Forebrain connections of the hamster intergeniculate leaflet: comparison with those of ventral lateral geniculate nucleus and retina. Vis Neurosci 16:1037-1054.
44. Morin LP, Blanchard JH. 2001. Neuromodulator content of hamster intergeniculate leaflet neurons and their projection to the suprachiasmatic nucleus or visual midbrain. J Comp Neurol 437:79-90.
45. Morin LP, Blanchard JH. 2005. Descending projections of the hamster intergeniculate leaflet: relationship to the sleep/arousal and visuomotor systems. J Comp Neurol 487:204-216.
46. Morin LP, Studholme KM. 2011. Separation of function for classical and ganglion cell photoreceptors with respect to circadian rhythm entrainment and induction of photosomnolence. Neuroscience 199:213-224.
47. Morin LP, Wood RI. 2001. A stereotaxic atlas of the hamster brain. New York: Academic Press. p 1-146.
48. Muscat L, Huberman AD, Jordan CL, Morin LP. 2003. Crossed and uncrossed retinal projections to the hamster circadian system. J Comp Neurol 466:513-524.
49. Nakagawa S, Mizuma M, Kuchiiwa S. 1998. The retinal projections to the ventral and dorsal divisions of the medial terminal nucleus and mesencephalic reticular formation in the Japanese monkey (Macaca fuscata): a reinvestigation with cholera toxin B subunit as an anterograde tracer. Brain Res 809:198-203.
50. Noseda R, Burstein R. 2011. Advances in understanding the mechanisms of migraine-type photophobia. Curr Opin Neurol 24:197-202.
51. Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, Burstein R. 2010. A neural mechanism for exacerbation of headache by light. Nat Neurosci 13:239-245.
52. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, Hogenesch JB, Provencio I, Kay SA. 2002. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213-2216.
53. Paul MJ, Indic P, Schwartz WJ. 2011. A role for the habenula in the regulation of locomotor activity cycles. Eur J Neurosci 34:478-488.
54. Paxinos G, Franklin KBJ. 2004. The mouse brain in stereotaxic coordinates. Amsterdam, Boston: Elsevier Academic Press.
55. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. New York: Academic Press.
56. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. New York: Academic Press.
57. Pemberton HR. 1891. Recent investigations on the structure and relations of the optic thalami. J Comp Neurol 1:135-148.
58. Pickard GE. 1985. Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus. Neurosci Lett 55:211-217.
59. Pickard GE, Silverman AJ. 1981. Direct retinal projections to hypothalamus, piriform cortex and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horseradish peroxidase technique. J Comp Neurol 196:155-172.
60. Pieper DR, Tang YK, Lipski TP, Subramanian MG, Newman SW. 1984. Olfactory bulbectomy prevents the gonadal regression associated with short photoperiod in male golden-hamsters. Brain Res 321:183-186.
61. Power BD, Leamey CA, Mitrofanis J. 2001. Evidence for a visual subsector within the zona incerta. Vis Neurosci 18:179-186.
62. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. 1998. Melanopsin: An opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95:340-345.
63. Raitiere MN, Garyfallou VT, Urbanski HF. 1995. Lesions in the bed nucleus of the stria terminalis, but not in the lateral septum, inhibit short-photoperiod-induced testicular regression in Syrian hamsters. Brain Res 705:159-167.
64. Rodieck RW. 1998. The first steps in seeing. Sunderland, MA: Sinauer Associates. p 1-562.
65. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. 2010. Sleep state switching. Neuron 68:1023-1042.
66. Scalia F, Arango V. 1979. Topographic organization of the projections of the retina to the pretectal region in the rat. J Comp Neurol 186:271-292.
67. Schmidt TM, Do MTH, Dacey D, Lucas R, Hattar S, Matynia A. 2011. Melanopsin-positive intrinsically photosensitive retinal ganglion cells: from form to function. J Neurosci 31:16094-16101.
68. Sefton AJ, Dreher B. 1995. Visual system. In: Paxinos G, editor. The rat nervous system. Vol 2. New York: Academic Press. p 833-898.
69. Sherman SM, Guillery RW. 1996. Functional organization of thalamocortical relays. J Neurophysiol 76:1367-1395.
70. Simpson JI, Leonard CS, Soodak RE. 1988. The accessory optic-system - analyzer of self-motion. N Y Acad Sci 545:170-179.
71. Soodak RE, Simpson JI. 1988. The accessory optic-system of rabbit. 1. Basic visual response properties. J Neurophysiol 60:2037-2054.
72. Stein BE, Merideth 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.
73. Stein BE, Rowland BA. 2011. Organization and plasticity in multisensory integration: early and late experience affects its governing principles. Prog Brain Res 191:145-163.
74. Studholme KM, Gompf HS, Morin LP. 2013. Brief light stimulation during the mouse nocturnal activity phase simultaneously induces a decline in core temperature and locomotor activity followed by EEG-determined sleep. Am J Physiol Regul Integr Comp Physiol 304:R459-R471.
75. Tan HS, Vandersteen J, Simpson JI, Collewijn H. 1993. 3-Dimensional organization of optokinetic responses in the rabbit. J Neurophysiol 69:303-317.
76. Uchiumi O, Sugita S, Fukuta K. 1995. Retinal projections to the subcortical nuclei in the Japanese field vole (Microtus-montebelli). Exp Anim 44:193-203.
77. Wagner CK, Silverman AJ, Morrell JI. 1998. Evidence for estrogen receptor in cell nuclei and axon terminals within the lateral habenula of the rat: regulation during pregnancy. J Comp Neurol 392:330-342.
78. Walker DL, Davis M. 1997. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17:9375-9383.
79. Zhao H, Rusak B. 2005. Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience 132:519-528.