Abstract
During development, retinal ganglion cell axons establish a topographically ordered projection from the retina to the superior colliculus (SC). The putative guidance activities for retinal axons that operate during embryonic development are not detectable in the normal adult SC. However, these cues reappear upon transection of the optic nerve of adult rats. In the present study, we used a modified version of the "stripe assay," in which membranes from either anterior or posterior SC alternated with laminin stripes. Temporal embryonic retinal axons consistently avoid membranes from embryonic posterior SC, but only rarely from adult deafferented SC. However, they are attracted to membranes from both embryonic and adult deafferented anterior SC. Nasal retinal axons only show a significant preference for membranes from posterior SC after deafferentation. When retinal axons were offered a choice to grow on membranes either from their embryonic or their deafferented target regions, they showed a preference for the deafferented SC. On carpets consisting of laminin and membranes from normal SC (not deafferented) or nontarget regions (inferior colliculus), temporal and nasal axons grow either in a random fashion or show preferences for the laminin stripes. Our modified version of the classic stripe assay shows specific growth preferences of embryonic retinal axons for membrane lanes from their appropriate embryonic or deafferented adult target regions. These findings suggest that the deafferentation of the SC in adult rats triggers the reexpression of specific guidance activities for retinal axons. Those "attractive" guidance cues appear to be differentially expressed in the developing and deafferented SC.
MeSH Terms
Afferent Pathways/embryology,physiology
Animals
Axons/physiology
Cues
Denervation
Female
Laminin
Membranes
Rats/embryology
Rats, Sprague-Dawley
Reference Values
Retinal Ganglion Cells/physiology,ultrastructure
Superior Colliculi/embryology,physiology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bähr M
Neurologische Universitätsklinik, Tübingen, Germany.
Wizenmann A
References (24)
24 references, click to expand
-
Regenerating retinal axons of goldfish respond to a repellent guiding component on caudal tectal membranes of adult fish and embryonic chick.
J Comp Neurol. 1991 Sep 15;311(3):321-9
PMID: 1659590
-
In vitro regeneration of adult rat ganglion cell axons from retinal explants.
Exp Brain Res. 1988;73(2):393-401
PMID: 3265109
-
Regenerating adult rat retinal axons reconnect with target neurons in-vitro.
Neuroreport. 1991 Oct;2(10):581-4
PMID: 1661620
-
Plasticity in the development of topographic order in the mammalian retinocollicular projection.
Dev Biol. 1994 Apr;162(2):384-93
PMID: 8150202
-
Guidance and induction of branch formation in developing axons by target-derived diffusible factors.
Curr Opin Neurobiol. 1995 Feb;5(1):83-90
PMID: 7773010
-
How do retinal axons find their targets in the developing brain?
Trends Neurosci. 1991 Jun;14(6):224-8
PMID: 1716013
-
Development of topographic order in the mammalian retinocollicular projection.
J Neurosci. 1992 Apr;12(4):1212-32
PMID: 1313491
-
Cross-species recognition of tectal cues by retinal fibers in vitro.
Development. 1989 Jun;106(2):313-20
PMID: 2591317
-
Control of topographic retinal axon branching by inhibitory membrane-bound molecules.
Science. 1994 Aug 5;265(5173):799-803
PMID: 8047886
-
Guidance and topographic stabilization of nasal chick retinal axons on target-derived components in vitro.
Neuron. 1993 Mar;10(3):345-57
PMID: 8461131
-
Goldfish retinal axons respond to position-specific properties of tectal cell membranes in vitro.
Neuron. 1989 Apr;2(4):1331-9
PMID: 2627373
-
Biochemical characterization of a putative axonal guidance molecule of the chick visual system.
Neuron. 1990 Nov;5(5):735-43
PMID: 2171592
-
Behavior of fish retinal growth cones encountering chick caudal tectal membranes: a time-lapse study on growth cone collapse.
J Neurobiol. 1993 Jan;24(1):37-50
PMID: 8419523
-
Antibody that neutralizes myelin-associated inhibitors of axon growth does not interfere with recognition of target-specific guidance information by rat retinal axons.
J Neurobiol. 1996 Jun;30(2):281-92
PMID: 8738756
-
Avoidance of posterior tectal membranes by temporal retinal axons.
Development. 1987 Dec;101(4):909-13
PMID: 3503703
-
Initial stages of retinofugal axon development in the hamster: evidence for two distinct modes of growth.
Exp Brain Res. 1991;87(2):371-82
PMID: 1722759
-
Appearance of target-specific guidance information for regenerating axons after CNS lesions.
Neuron. 1993 Nov;11(5):975-83
PMID: 8240818
-
In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases.
Cell. 1995 Aug 11;82(3):359-70
PMID: 7634326
-
Perspectives on axonal regeneration in the mammalian CNS.
Trends Neurosci. 1994 Nov;17(11):473-9
PMID: 7531889
-
Formation of functional synapses by regenerating adult rat retinal ganglion cell axons in midbrain target regions in vitro.
J Neurobiol. 1993 Apr;24(4):456-73
PMID: 8515251
-
Responses of retinal axons in vivo and in vitro to position-encoding molecules in the embryonic superior colliculus.
Neuron. 1992 Nov;9(5):977-89
PMID: 1419004
-
Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro.
Development. 1987 Dec;101(4):685-96
PMID: 3503693
-
The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons.
Dev Biol. 1987 Aug;122(2):407-18
PMID: 2954871
-
Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading.
J Cell Biol. 1988 Apr;106(4):1281-8
PMID: 3360853