Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T09:47:51.796Z Has data issue: false hasContentIssue false
  • English
  • Français

Compensation for population size mismatches in the hamster retinotectal system: Alterations in the organization of retinal projections

Published online by Cambridge University Press:  02 June 2009

S.L. Pallas  and
B.L. Finlay
S.L. Pallas
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
B.L. Finlay
Affiliation:
Department of Psychology, Cornell University, Ithaca
Get access Rights & Permissions [Opens in a new window]

Abstract

Unilateral partial ablation of the superior colliculus in the hamster results in a compression of the retinotopic map onto the remaining tectal fragment. In a previous electrophysiological study (Pallas & Finlay, 1989a), we demonstrated that receptive-field properties of single tectal units (including receptive-field size) remain unchanged, despite the increased afferent/target convergence ratios in the compressed tecta. The present study was done to investigate the mechanism that produces increased convergence from retina to tectum at the population level while maintaining apparent stability of convergence at the single neuron level. We injected comparable quantities of horseradish peroxidase into the tecta of normal adult hamsters and adult hamsters that had received neonatal partial tectal ablations of varying magnitude. We then compared the area of retina backfilled from the injection and the number and density of labeled retinal ganglion cells within it to the size of the remaining tectal fragment.

As expected from earlier anatomical (Jhaveri & Schneider, 1974) and physiological (Finlay et al., 1979a; Pallas & Finlay, 1989a) studies demonstrating compression of the retinotectal projection, we found that the area of retina labeled from a single tectal injection site increases linearly with decreasing tectal fragment size. However, for fragment sizes down to 30% of normal, total number of retinal ganglion cells projecting to the injection site remains in or above the normal range. For large lesions (less than 30% of tectum remaining), total number of labeled retinal ganglion cells declines from normal, despite the fact that a larger absolute area of retina is represented on each unit of tectum under these conditions. Comparison of retinal ganglion cell density with tectal fragment size shows an initial decline with decreasing fragment size, which becomes sharper with very large lesions (small tectal fragments).

The maintenance of the normal number of retinal ganglion cells innervating each patch of tectum could be accomplished by an elimination of the tectal collaterals of some retinal ganglion cells. Our results suggest that, in addition to collateral elimination, reduction in the size of ganglion cell arbors is occurring, since the peak density of backfilled ganglion cells declines less rapidly than backfilled retinal area increases, especially for small lesions. However, arbor reduction and collateral elimination must occur in such a way that individual tectal cells represent the same amount of visual space as normal.

Thus, collateral elimination and arbor reduction are two mechanisms that operate to maintain afferent/target convergence ratios (and thus receptive-field properties) over large variations in afferent availability. This compensation may occur through an activity-dependent stabilization mechanism that does not change its selectivity even when excess afferents are available. For very large lesion sizes, receptive-field size and innervating ganglion cell number and density are not preserved, thus demonstrating a limit to the afferent/target matching mechanism. The same ontogenetic mechanisms might provide a buffer for normal variations in afferent populations, and could help to align topographic maps with differing numbers of afferents.

Keywords

Superior colliculusAfferent/target matchingCollateral eliminationNeonatal lesionsRetinal ganglion cell
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 3 , March 1991 , pp. 271 - 281
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bastian, J. (1982). Vision and electroreseption: integration of sensory information in the optic of the weakly electric fish (Apteronotue albifrons). Journal of Comparative Physiology 147, 287–297.CrossRefGoogle Scholar
Cline, H.T. & Constantine-Paton, M. (1989). NMDA receptor anrtagonists disrupt the retinotectal topographic map. Neuron. 3, 413–426.CrossRefGoogle ScholarPubMed
Crain, B.J. & Hall, W.C. (1980a). The organization of the lateral posterior nucleus of the golden hamster after neonatal superior colliculus lesions. Journal of Comparative Neurology 193, 383–401.CrossRefGoogle ScholarPubMed
Carin, B.J. & Hall, W.C. (1980b). The organiation of the lateral posterior nuleus of the golden hamster after different combinations of neonatal lesions. Journal of Comparative Neurology 193, 403–412.CrossRefGoogle Scholar
Finlay, B.L. (1979). Experimental manipulations of the development of ordered projections in the mammalian brain. In Development Neurobiology of Vision, ed. Freeman, R.A., pp. 391–402. New York: Plenum Press.CrossRefGoogle Scholar
Finaly, B.L. & Pallas, S.L. (1989). Afferent/target mismatches in the mammalian retinotectal system are balanced by changes in retinal axon arborization and projection patterns. Society for Neuroscience Abstracts 15, 1212.Google Scholar
Finaly, B.L., Schneps, S.E. & Schneider, G.E. (1979a). Orderly compression of the retinotectal projection following partial tectal ablation in the newborn hamster. Nature 280, 153–154.CrossRefGoogle Scholar
Finaly, B.L., Wilson, K.G. & Schneider, G.E. (1979b). Anomalous ipsilateral retinal projections in Syrian hamsters with neonatal lesions: topography and functional capacity. Journal of Comparative Neurology 183, 721–740.CrossRefGoogle Scholar
Finaly, B.L., Schneps, S.E., Wilson, K.G. & Schneider, G.E. (1978). Topography of visual and somatosensory projections to the superior colliculus of the golden hamster. Brain Research 142, 223–235CrossRefGoogle Scholar
Gottlieb, M.D., Pasik, P. & Pasik, T. (1985). Early postnatal development of the monkey visual system I: Growth of the lateral geniculate nucleus and striate cortex. Developmental Brain Research 17, 53–62.CrossRefGoogle Scholar
Hartline, P.H. (1984). The optic tectum of reptiles: neurophysiological studies. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 601–618. New York: Plenum Press.CrossRefGoogle Scholar
Hayes, W.P. & Meyer, R.L. (1988). Optic synapse number but not density is constrained during regeneration onto surgically halved tectum in goldfish: HRP-EM evidence that optic fibers compete for fixed numbers of postsynaptic sites on the tectum. Journal of Comparative Neurology 274, 539–559.CrossRefGoogle Scholar
Jhaveri, S.R. & Schneider, G.E. (1974). Neuroanatomical correlates of spared or altered function after brain lesions in the newborn hamster. In Plasticity and Recovery of Function in the Central Nervous System ed. Stein, D.G., Rosen, J.J. & Butters, N. pp. 65–109.Google Scholar
Knudsen, E.I. (1982). Auditory and visiual and visual maps of space in the optic tectum of the owl. Journal of Neuroscience, 2, 1177–1194.CrossRefGoogle Scholar
Meyer, R.L., Sakurai, K. & Schauwecker, E. (1985). Topography of regenerating optic fibers in goldfish traced with local wheat-germ injections into retina: evidence for discontinuous microtopography in the retinotectal projection. Journal of Comparative Neurology 239, 27–43.CrossRefGoogle ScholarPubMed
Murray, M., Sharma, S. & Edwards, M.A. (1982). Target regulation of synaptic number in the compressed retinotectal projection of goldfish. Journal of Comparative Neurology 209, 374–385.CrossRefGoogle ScholarPubMed
Pallas, S.L. & Finlay, B.L. (1989a). Conservation of receptive-field properties of superior colliculus cells after development reassangements of retinal input, Visual Neurosience 2, 121–135.CrossRefGoogle ScholarPubMed
Pallas, S.L. & Finlay, B.L. (1989b). Changes in axonal arborization patterns can compensate for mismatches in size of innervating and target populations in the mammalian retinotectal system. Proceedings in the Congress on Neuroethology 2, 200A.Google Scholar
Perry, V.H. & Cowey, A. (1979). The effects of unilateral cortica and tectal lesions on retinal ganglion cells in rats. Experimental Brain Research 35, 97–108.CrossRefGoogle Scholar
Rankin, E.C.C. & Cook, J.K. (1986). Topographic refinement of the regenerating retinotectal projection of the goldfish in standard laboratory conditions: a quantiatative WGA-HRP study. Experimental Brain Research 63, 409–420.CrossRefGoogle Scholar
Schneider, G.E. (1970). Mechanisms of functional recovery following lesions of visual cortex or colliculus in neonate and adult hamsters. Behavior and Evolution 3, 295–323.CrossRefGoogle ScholarPubMed
Schneider, G.E. (1973). Early lesions of the superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behavior and Evolution, 8, 73–109.CrossRefGoogle ScholarPubMed
Sengelaub, D.R., Windrem, M.S. & Finlay, B.L. (1983). Alterations of adult retinal ganglion cell distribution following early monocular enucleation. Experimental Brain Research 52, 269–276.Google Scholar
Sperry, D.G. (1987). Relationship between natural variations in motoneuron numcer and body size in Xenopus laevis: atest for size matching. Journal of Comparative Neurology 264, 250–267.CrossRefGoogle Scholar
Stein, B.E., Magalhaes-Castro, B. & Keuger, L. (1975). Superior colliculus: visuotopic-somatotopicoverlap. Science 189, 224–226.CrossRefGoogle Scholar
Udin, S.B. & Schneider, G.E. (1981). Compressed retinotectal projection in hamsters: fewer ganglion cells project to tectum after neonatal tectal lesion. Experimental Brain Research 43, 261–269.Google Scholar
Wikler, K.C. & Finlay, B.L. (1984). Deafferentation of the superior collicluus results in decreased synaptic density. Society for Neuroscience Abstracts 10, 462.Google Scholar
Wikler, K.C. & Finlay, B.L. (1989). Development heterochrony and the evolution of species differences in retinal specializations. In Development of the Vertebrate Retina, ed. Finlay, B.L. & Sengelaub, D.R., pp. 227–246. New York: Plenum.CrossRefGoogle Scholar
Wikler, K.C., Kirn, J., Windrem, M.S. & Finaly, B.L. (1986). Control of cell number in the developing visual system, III: Partial tectal ablation. Development Brain Research 28, 23–32.CrossRefGoogle Scholar