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An examination of linking hypotheses drawn from the perceptual consequences of experimentally induced changes in neural circuitry

Published online by Cambridge University Press:  07 August 2013

DONALD E. MITCHELL*
Affiliation:
Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada
STEPHEN G. LOMBER
Affiliation:
Brain and Mind Institute, Department of Psychology, University of Western Ontario, London, Ontario, Canada
*
*Address correspondence to: Dr. Donald E. Mitchell, Department of Psychology and Neuroscience, Dalhousie University, Life Sciences Centre, Halifax, Nova Scotia, B3H 4R2, Canada. E-mail: d.e.mitchell@dal.ca

Abstract

Because targeted early experiential manipulations alter both perception and the response properties of particular cells in the striate cortex, they have been used as evidence for linking hypotheses between the two. However, such hypotheses assume that the effects of the early biased visual input are restricted to just the specific cell population and/or visual areas of interest and that the neural populations that contribute to the visual perception itself do not change. To examine this assumption, we measured the consequences for vision of an extended period of early monocular deprivation (MD) on a kitten (from 19 to 219 days of age) that began well before, and extended beyond, bilateral ablation of visual cortical areas 17 and 18 at 132 days of age. In agreement with previous work, the lesion reduced visual acuity by only a factor of two indicating that the neural sites, other than cortical areas 17 and 18, that support vision in their absence have good spatial resolution. However, these sites appear to be affected profoundly by MD as the effects on vision were just as severe as those observed following MD imposed on normal animals. The pervasive effects of selected early visual deprivation across many cortical areas reported here and elsewhere, together with the potential for perception to be mediated at a different neural site following deprivation than after typical rearing, points to a need for caution in the use of data from early experiential manipulations for formulation of linking hypotheses.

Type
Linking performance and neural mechanisms in development and disability
Copyright
Copyright © Cambridge University Press 2013 

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References

Barnes, G.R., Hess, R.F., Dumoulin, S.O., Achtman, R.L. & Pike, G.B. (2001). The cortical deficit in humans with strabismic amblyopia. The Journal of Physiology 533, 281297.CrossRefGoogle ScholarPubMed
Beaver, B.V., Reed, W., Leary, S., McKiernan, B., Bain, F., Schultz, R., Bennett, B.T., Pascoe, P., Schull, E., Cork, L.C., Francis-Floyd, R., Amass, K.D., Johnson, R.J., Schmidt, R.H., Underwood, W., Thorton, G.W. & Kohn, B. (2001). 2000 Report of the AVMA Panel of Euthanasia. Journal of the American Veterinary Medical Association 218, 669696.Google Scholar
Berkley, M.A. & Sprague, J.M. (1979). Striate cortex and visual acuity functions in the cat. The Journal of Comparative Neurology 187, 679702.CrossRefGoogle ScholarPubMed
Cynader, M. & Chernenko, G. (1976). Abolition of direction selectivity in the visual cortex of the cat. Science 193, 504505.CrossRefGoogle ScholarPubMed
Doty, R.W. (1967). The misnomer “lateral gyrus” in lieu of “marginal gyrus” in the cat. Experimental Neurology 17, 263264.CrossRefGoogle Scholar
El-Shamayleh, Y., Kiorpes, L., Kohn, A. & Movshon, J.A. (2010). Visual motion processing by neurons in area MT of macaque monkeys with experimental amblyopia. The Journal of Neuroscience 30, 1219812209.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1970). The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: A new interpretation. The Journal of Comparative Neurology 138, 339368.CrossRefGoogle Scholar
Hedges, J.H., Gartshteyn, Y., Kohn, A., Rust, N.C., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (2011). Dissociation of neuronal and psychophysical responses to local and global motion. Current Biology: CB 21, 20232028.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. The Journal of Physiology 160, 106154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. The Journal of Physiology 195, 215243.CrossRefGoogle ScholarPubMed
Kalia, M. & Whitteridge, D. (1973). The visual areas in the splenial sulcus of the cat. The Journal of Physiology 232, 275283.CrossRefGoogle ScholarPubMed
Kaye, M., Mitchell, D.E. & Cynader, M. (1981). Selective loss of binocular depth perception after ablation of cat visual cortex. Nature 292, 6062.CrossRefGoogle Scholar
Kiorpes, L., Kiper, D.C., O’Keefe, L.P., Cavanaugh, J.R. & Movshon, J.A. (1998). Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. The Journal of Neuroscience 15, 64116424.CrossRefGoogle Scholar
Kiorpes, L. & McKee, S.P. (1999). Neural mechanisms underlying amblyopia. Current Opinion in Neurobiology 9, 480486.CrossRefGoogle ScholarPubMed
Lehmkuhle, S, Kratz, K.E. & Sherman, S.M. (1982). Spatial and temporal sensitivity of normal and amblyopic cats. Journal of Neurophysiology 48, 372387.CrossRefGoogle ScholarPubMed
Lerner, Y., Pianka, P., Azmon, B., Leiba, H., Stolovich, C., Loewenstein, A., Harel, M., Hendler, T. & Malach, R. (2003). Area-specific amblyopic effects in human occipitotemporal object representations. Neuron 40, 10231029.CrossRefGoogle ScholarPubMed
Li, X., Dumoulin, S.O., Mansouri, B. & Hess, R.F. (2007). Cortical deficits in human amblyopia: Their regional distribution and their relationship to the contrast detection deficit. Investigative Ophthalmology & Visual Science 48, 15751591.CrossRefGoogle Scholar
Lomber, S.G., Payne, B.R., Cornwell, P. & Pearson, H.E. (1993). Capacity of the retinogeniculate pathway to reorganize following ablation of visual cortical area in developing and mature cats. The Journal of Comparative Neurology 338, 432457.CrossRefGoogle ScholarPubMed
Lomber, S.G., MacNeil, M.A. & Payne, B.R. (1995). Amplification of thalamic projections to middle suprasylvian cortex following ablation of immature primary visual cortex in the cat. Cerebral Cortex 5, 166191.CrossRefGoogle ScholarPubMed
Mitchell, D.E. (1988). The extent of visual recovery from early monocular or binocular visual deprivation in kittens. The Journal of Physiology 395, 639660.CrossRefGoogle ScholarPubMed
Mitchell, D.E. (2002). Behavioral analyses of the contributions of cat primary visual cortex to vision. In The Cat Primary Visual Cortex, ed. Payne, B.R. & Peters, A., pp. 655691. San Diego, CA: Academic Press.CrossRefGoogle Scholar
Mitchell, D.E. (2004). The effects of selected forms of early visual deprivation on perception. In The Visual Neurosciences, Vol. 1, ed. Chalupa, L.M. & Werner, J.S., pp. 189204. Cambridge, MA: MIT Press.Google Scholar
Mitchell, D.E., Giffin, F. & Timney, B. (1977). A behavioral technique for the rapid assessment of the visual capabilities of kittens. Perception 6, 181193.CrossRefGoogle ScholarPubMed
Murphy, K.M. & Mitchell, D.E. (1987). Reduced visual acuity in both eyes of monocularly deprived kittens following a short or long period of reverse occlusion. The Journal of Neuroscience 7, 15261536.CrossRefGoogle ScholarPubMed
Olfert, E., Cross, B.M. & McWilliam, A.A. (1993). Guide to the Care and Use of Experimental Animals. Ottawa, ON: Canadian Council on Animal Care.Google Scholar
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 1721.CrossRefGoogle ScholarPubMed
Palmer, L.A., Rosenquist, A.C. & Tusa, R.J. (1978). The retinotopic organization of lateral suprasylvian visual areas in the cat. The Journal of Comparative Neurology 177, 237256.CrossRefGoogle ScholarPubMed
Pasternak, T. (1986). The role of cortical directional selectivity in detection of motion and flicker. Vision Research 26, 11871194.CrossRefGoogle ScholarPubMed
Pasternak, T., Schumer, R.A., Gizzi, M.S. & Movshon, J.A. (1985). Abolition of visual cortical direction selectivity affects visual behavior in cats. Experimental Brain Research 61, 214217.CrossRefGoogle ScholarPubMed
Reinoso-Suárez, F. (1961). Topographischer Hirnatlas der Katz für experimentale physiologische Untersuchungen. [Topographical atlas of the cat brain for experimental-physiological research]. Darmstad, Federal Republic of Germany: Merck.Google Scholar
Rosenquist, A.C. (1985). Connections of visual cortical areas in the cat. In: Cerebral Cortex: Visual Cortex, Vol. 3, ed. Peters, A. & Jones, E.G., pp 81117. New York, NY: Plenum.Google Scholar
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. The Journal of Comparative Neurology 143, 101118.CrossRefGoogle Scholar
Schröder, J.-H., Fries, P., Roelfsema, P.R., Singer, W. & Engel, A.K. (2002). Ocular dominance in extrastriate cortex of strabismic amblyopic cats. Vision Research 42, 2939.CrossRefGoogle ScholarPubMed
Sherman, S.M. (1985). Functional organization of the W-, X-, and Y-cell pathways in the cat: A review and hypothesis. In Progress in Psychobiology and Physiological Psychology, Vol. 11, ed. Sprague, J.M. & Epstein, A.N., pp. 233314. New York, NY: Academic.Google Scholar
Sireteanu, R. & Best, J. (1992). Squint-induced modification of visual receptive fields in the lateral suprsylvian cortex of the cat: Binocular interaction, vertical effect and anomalous correspondence. The European Journal of Neuroscience 4, 235242.CrossRefGoogle Scholar
Tretter, F., Cynader, M. & Singer, W. (1975). Organization of cat parastriate cortex: A primary or secondary visual area. Journal of Neurophysiology 38, 10991113.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. The Journal of Comparative Neurology 177, 213235.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1981). Multiple cortical visual areas: Visual field topography in the cat. In Cortical Sensory Organization: Multiple Visual Areas, Vol. 2, ed. Woolsey, C.N., pp. 131. Clifton, NJ: Humana Press.Google Scholar
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. The Journal of Comparative Neurology 185, 657678.CrossRefGoogle Scholar