Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-26T12:02:48.109Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurotrophic and behavioral effects of occipital cortex transplants in newborn rats

Published online by Cambridge University Press:  02 June 2009

Get access Rights & Permissions [Opens in a new window]

Abstract

Cell suspensions of embryonic occipital cortex were transplanted into newborn rats with large unilateral visual cortex lesions. When the animals were adults, they were tested on a difficult visual discrimination, and subsequently their brains were analyzed for possible neurotrophic effects of the transplants on nonvisual cortical areas which normally form connections with the occipital cortex. Behaviorally, animals with lesions and transplants learn to discriminate between columns and rows of squares at a rate which is identical to normal rats while animals with lesions and no transplants are impaired. Volume and cell-density measures show that the transplants also rescue neurons in cortical area 8 that would normally degenerate following the cortical lesion. No such neurotrophic effect of the transplants is found in cortical area 24 or area 17 contralateral to the lesion. In rats with lesions and no transplants, there is a significant correlation between the amount of area 8 remaining after the lesion and trials to criterion on the columns-rows discrimination, a relationship that does not exist in transplant animals because of their normal learning curve and the consistent sparing of area 8. Injections of HRP into the visual cortex contralateral to the lesion result in variable numbers of labeled cells within the transplant. However, there is no consistent relationship between the number of transplant cells which project to the opposite hemisphere and learning of the discrimination. It is suggested that the learning deficit following the lesion is largely attentional and that the sparing of cortical area 8 (which in rats may include the analog of the frontal eye fields present in the primate cortex) contributes to the sparing of function.

Keywords

Visual cortexCNS transplantsVisual pattern discriminationNeurotrophic interactionsMedial frontal cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 2 , Issue 2 , February 1989 , pp. 189 - 198
Copyright
Copyright © Cambridge University Press 1989

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

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 238–248.CrossRefGoogle ScholarPubMed
Arendash, G.W. & Gorski, R.A. (1982). Enhancement of sexual behavior in female rats by neonatal transplantation of brain tissue from males. Science 217, 1267–1278.CrossRefGoogle ScholarPubMed
Barbas, H. & Spear, P.D. (1976). Effects of serial unilateral and serial bilateral visual cortex lesions on brightness discrimination relearning in rats. Journal of Comparative Psychology 90, 279–292.Google ScholarPubMed
Bartus, R.T. (1987). Neural tissue transplantation; comments on its role in general neuroscience and its potential as a therapeutic approach. In Cell and Tissue Transplantation Into the Adult Brain, ed. Azmitia, E.C. & Bjorklund, A., pp. 355–361. New York: New York Academy of Sciences.Google Scholar
Bjorklund, A., Dunnett, S.B., Stenevi, U., Lewis, M.E. & Iversen, S.D. (1980). Reinnervation of the denervated striatum by substantia nigra transplants: functional consequences as revealed by pharmacological and sensorimotor testing. Brain Research 199, 307–333.CrossRefGoogle ScholarPubMed
Bleier, R. (1969). Retrograde transsynaptic cellular degeneration in mammilary and ventral tegmental nuclei following limbic decortication in rabbits of various ages. Brain Research 15, 365–393.CrossRefGoogle Scholar
Brundin, P., Barbin, G., Issacson, O., Mallat, M., Chamak, B., Prochiantz, A., Gage, F.H. & Bjorklund, A. (1985). Survival of intracerebrally grafted rat dopamine neurons previously cultured in vitro. Neuroscience Letters 61, 79–84.CrossRefGoogle ScholarPubMed
Buchanan, J.T. & Nornes, H.O. (1986). Transplants of embryonic brainstem containing the locus coeruleus into spinal cord enhance the hindlimb flexion reflex in adult rats. Brain Research 381, 225–236.CrossRefGoogle ScholarPubMed
Butler, H. & Juurlink, B.H.J. (1987). An Atlas for Staging Mammalian and Chick Embryos. Boca Raton, Florida: CRC Press.Google Scholar
Castro, A.J., Zimmer, J., Sunde, N.A.A. & Bold, E.L. (1985). Transplantation of fetal cortex to the brain of newborn rats: a retrograde fluorescent analysis of callosal and thalamic projections from transplant to host. Neuroscience Letters 60, 283–288.CrossRefGoogle Scholar
Caviness, V.S. Jr, (1975). Architectonic map of neocortex of the normal mouse. Journal of Comparative Neurology 164, 247–264.CrossRefGoogle ScholarPubMed
Chang, F.L.F., Steedman, J.G. & Lund, R.D. (1986). The lamination and connectivity of embryonic cerebral cortex transplanted into newborn rat cortex. Journal of Comparative Neurology 244, 401–411.CrossRefGoogle ScholarPubMed
Christie, D. & Steele Russell, I. (1985 a). Visuomotor strategies in pattern discrimination learning in rats. Behavioural Brain Research 16, 9–18.CrossRefGoogle ScholarPubMed
Christie, D. & Steele Russell, I. (1985 b). Frontal eye field lesions: ocular or field neglect? Behavioural Brain Research 16, 198.CrossRefGoogle Scholar
Corwin, J.V., Kanter, S., Watson, R.T., Heilman, K.M., Valenstein, E. & hashimoto, A. (1986). Apomorphine has a therapeutic effect on neglect produced by unilateral dorsomedial prefrontal cortex lesions in rats. Experimental Neurology 94, 683–698.CrossRefGoogle Scholar
Cowey, A. & Bozek, T. (1974). Contralateral “neglect” after unilateral dorsomedial prefrontal lesions in rats. Brain Research 72, 53–63.CrossRefGoogle ScholarPubMed
Crowne, D.P., Yeo, C.H. & Steele Russell, I. (1981). The effects of unilateral frontal eye field lesions in the monkey–visual motor guidance and avoidance behavior. Behavioural Brain Research 2, 165–187.CrossRefGoogle Scholar
Cunningham, T.J., Sutilla, C.B. & Haun, F. (1987 b). Trophic effects of transplants following damage to the cerebral cortex. In Cell and Tissue Transplantation Into the Adult Brain, ed. Azmitia, E.C. & Bjorklund, A., pp. 153–168. New York: New York Academy of Sciences.Google Scholar
Cusick, C.G. & Lund, R.D. (1981). The distribution of the callosal projections to the occipital visual cortex in rats and mice. Brain Research 214, 239–259.CrossRefGoogle Scholar
Dean, P. (1981). Visual pathways and acuity in hooded rats. Behavioural Brain Research 3, 239–271.CrossRefGoogle ScholarPubMed
Dunnett, S.B., Low, W.C., Iversen, S.D., Stenevi, U. & Bjorklund, A. (1982). Septal transplants restore maze learning in rats with fornix-fimbria lesions. Brain Research 251, 335–348.CrossRefGoogle ScholarPubMed
Dunnett, S.B., Toniolo, G., Fine, A., Ryan, C.N., Bjorklund, A. & Iversen, S.D. (1985). Transplantation of embryonic ventral forebrain neurons to the neocortex of rats with lesions of the nucleus basalis magnocellularis-II. Sensorimotor and learning impairments. Neuroscience 16, 787–797.CrossRefGoogle Scholar
Floeter, M.K. & Jones, E.J. (1984). Connections made by transplants to the cerebral cortex of rat brains damaged in utero. Journal of Neuroscience 4, 141–150.CrossRefGoogle Scholar
Floeter, M.K. & Jones, E.J. (1985). Transplantation of fetal postmitotic neurons to rat cortex: survival, early pathway choices, and long-term projections of outgrowing axons. Developmental Brain Research 22, 19–38.CrossRefGoogle Scholar
Freed, W.J. (1983). Functional brain tissue transplantation: reversal of lesion-induced rotation by intraventricular substantia nigra and adrenal medulla grafts, with a note on intracranial retinal grafts. Biological Psychiatry 18, 1205–1267.Google ScholarPubMed
Freed, W.J., Morihisa, J.M., Spoor, E., Hoffer, B.J., Olson, L., Sieger, A. & Wyatt, R.J. (1981). Transplanted adrenal chromaffin cells in rat brain reduce lesion-induced rotational behavior. Nature 292, 351–352.CrossRefGoogle Scholar
Freed, W.J., Perlow, M.J., Karoum, F., Seiger, A., Olson, L., Hoffer, B.J. & Wyatt, R.J. (1980). Restoration of dopaminergic function by grafting of fetal rat substantia nigra to the caudate nucleus: long-term behavioral, biochemical, and histochemical studies. Annals of Neurology 8, 510–519.CrossRefGoogle Scholar
Gage, F.H. & Bjorklund, A. (1986). Cholinergic septal grafts into the hippocampal formation improve spatial learning and memory in aged rats by an atropine-sensitive mechanism. Journal of Neuroscience 6, 2837–2847.CrossRefGoogle ScholarPubMed
Gage, F.H., Bjorklund, A., Stenevi, U., Dunnett, S.B. & Kelly, P.A.T. (1984). Intrahippocampal septal grafts ameliorate learning impairments in aged rats. Science 225, 533–536.CrossRefGoogle ScholarPubMed
Gash, D. & Sladek, J.R. (1980). Functional development of grafted vasopressin neurons. Science 210, 1367–1369.CrossRefGoogle ScholarPubMed
Gellerman, L.W. (1933). Chance order of alternating stimuli in visual discrimination experiments. Journal of Genetic Psychology 42, 207–208.Google Scholar
Gibbs, R.B., Yu, J. & Cotman, C.W. (1987). Entorhinal transplants and spatial memory abilities in rats. Behavioural Brain Research 26, 29–35.CrossRefGoogle ScholarPubMed
Gibson, A.R., Hansma, D.I., Houk, J.C. & Robinson, F.R. (1984). A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Research 298, 235–241.CrossRefGoogle ScholarPubMed
Goldstein, L.H. & Oakley, D.A. (1987). Visual discrimination in the absence of visual cortex. Behavioural Brain Research 24, 181–193.CrossRefGoogle ScholarPubMed
Haun, F. & Cunningham, T.J. (1984). Conical transplants reveal CNS trophic interactions in situ. Developmental Brain Research 15, 290–294.CrossRefGoogle Scholar
Haun, F. & Cunningham, T.J. (1986). Cortical transplants rescue dorsal lateral geniculate neurons after cortical lesions in adult hosts. Society for Neuroscience Abstracts 12, 588.Google Scholar
Haun, F. & Cunningham, T.J. (1987). Specific neurotrophic interactions between cortical and subcortical visual structures in developing rat: In vivo studies. Journal of Comparative Neurology 256, 561–569.CrossRefGoogle ScholarPubMed
Haun, F., Rothblat, L.A. & Cunningham, T.J. (1985). Visual cortex transplants in rats restore normal learning of a difficult visual pattern discrimination. Investigative Ophthalmology and Visual Science 263, 288.Google Scholar
Hendrickson, A. & Dineen, J.T. (1982). Hypertrophy of neurons in dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys. Neuroscience Letters 30, 217–222.CrossRefGoogle ScholarPubMed
Hsiao, C. & Fukuda, Y. (1984). Plastic changes in the distribution and soma size of retinal ganglion cells after neonatal monocular enucleation in rats. Brain Research 301, 1–12.CrossRefGoogle ScholarPubMed
Hughes, H.C. (1977). Anatomical and neurobehavioral investigations concerning the thalamo-cortical organization of the rat's visual system. Journal of Comparative Neurology 175, 311–336.CrossRefGoogle ScholarPubMed
Innocenti, G.M., Clarke, S. & Kraftsik, R. (1986). Interchange of callosal and association projections in the developing visual cortex. Journal of Neuroscience 6, 1384–1409.CrossRefGoogle ScholarPubMed
Ivy, G.O. & Killackey, H.P. (1982). Ontogenetic changes in the projections of neocortical neurons. Journal of Neuroscience 2, 735–743.CrossRefGoogle ScholarPubMed
Keating, E.G. (1980). Residual spatial vision in the monkey after removal of striate and preoccipital cortex. Brain Research 187, 271–290.CrossRefGoogle ScholarPubMed
Kesslak, J.P., Brown, L., Steichen, C. & Cotman, C.W. (1986 a). Adult and embryonic frontal cortex transplants after frontal cortex ablation enhance recovery on a reinforced alternation task. Experimental Neurology 94, 615–626.CrossRefGoogle ScholarPubMed
Kesslak, J.P., Nieto—Sampedro, M., Globus, J. & Cotman, C.W. (1986 b). Transplants of purified astrocytes promote behavioral recovery after frontal cortex ablation. Experimental Neurology 92, 377–390.CrossRefGoogle ScholarPubMed
Krieg, W.J.S. (1946). Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas. Journal of Comparative Neurology 84, 221–276; B. structure of the cortical areas. Journal of Comparative Neurology, 84, 277–284.CrossRefGoogle Scholar
Krieger, D.T., Perlow, M.J., Gibson, M.J., Davies, T.F., Zimmerman, E.A., Ferin, M. & Charleton, H.M. (1982). Brain grafts reverse hypogonadism of gonadotropin releasing hormone deficiency. Nature, 298, 468–471.CrossRefGoogle ScholarPubMed
Labbe, R., Firl, A., Mufson, E.J. & Stein, D.G. (1983). Fetal brain transplants: reduction of cognitive deficits in rats with frontal cortex lesions. Science 221, 470–472.CrossRefGoogle ScholarPubMed
Lashley, K.S. (1939). The mechanism of vision. XVI. The functioning of small remnants of the visual cortex. Journal of Comparative Neurology 70, 45–67.CrossRefGoogle Scholar
Lavond, D., Hata, H.G., Gray, T., Geckler, C.L., Meyer, P.M. & Meyer, D.R. (1978). Visual form perception is a function of the visual cortex. Physiological Psychology 6, 471–477.CrossRefGoogle Scholar
Low, W.C., Lewis, P.R., Bunch, S.T., Dunnett, S.B., Thomas, S.R., Iversen, S.D., Bjorklund, A. & Stenevi, U. (1982). Functional recovery following neural transplantation of embryonic septal nuclei in adult rats with septohippocampal lesions. Nature 300, 260–262.CrossRefGoogle ScholarPubMed
Lund, R.D., Land, P.W. & Boles, J. (1980). Normal and abnormal uncrossed retinotectal pathways in rats: an HRP study. Journal of Comparative Neurology 189, 711–720.CrossRefGoogle ScholarPubMed
McDaniel, W.F., Coleman, J. & Lindsay, J.F. Jr, (1982). A comparison of lateral peristriate and striate neocortical ablations in the rat. Behavioural Brain Research 6, 241–272.CrossRefGoogle ScholarPubMed
Mesulam, M.M. & Mufson, E.J. (1981). The rapid anterograde transport of horseradish peroxidase. Neuroscience 5, 1277–1286.CrossRefGoogle Scholar
Miller, M.W. & Vogt, B.A. (1984). Direct connections of rat visual cortex with sensory, motor and association cortices. Journal of Comparative Neurology 226, 184–202.CrossRefGoogle ScholarPubMed
Murphy, E.H., Mize, R.R. & Schecter, P.B. (1975). Visual discrimination following infant and adult ablation of cortical areas 17, 18, and 19 in the cat. Experimental Neurology 49, 386–405.CrossRefGoogle Scholar
Nilsson, O.G., Shapiro, M.L., Gage, F.H., Olton, D.S. & Bjorklund, A. (1987). Spatial learning and memory following fimbriafornix transection and grafting of fetal septal neurons to the hippocampus. Experimental Brain Research 67, 195–215.CrossRefGoogle ScholarPubMed
Olavarria, J. & Van Sluyters, R.C. (1985). Organization and postnatal development of callosal connections in the visual cortex of the rat. Journal of Comparative Neurology 239, 1–26.CrossRefGoogle ScholarPubMed
O'Leary, D.D.M., Stanfield, B.B. & Cowan, W.M. (1981). Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axonal collaterals rather than to the death of neurons. Developmental Brain Research 1, 607–617.CrossRefGoogle Scholar
Perenin, M.T. (1978). Visual function within the hemianopic field following early cerebral hemidecortication in man. II. Pattern discrimination. Neuropsychologia 16, 696–708.Google ScholarPubMed
Reep, R.L., Corwin, J.V., Hashimoto, A. & Watson, R.T. (1987). Efferent connections of the rostral portion of medial angranular cortex in rats. Brain Research Bulletin, 19, 203–221.CrossRefGoogle ScholarPubMed
Rothblat, L.A. & Hayes, L.L. (1982). Age-related changes in the distribution of visual callosal neurons following monocular enucleation in the rat. Brain Research 246, 146–149.CrossRefGoogle ScholarPubMed
Rothblat, L.A. & Schwartz, M.L. (1978). Complex pattern discrimination in the albino rat: role of striate cortex and the ipsilateral retinocortical pathway. Society for Neuroscience Abstracts 4, 643.Google Scholar
Rothblat, L.A., Schwartz, M.L. & Kasden, E.M. (1978). Monocular deprivation in the rat: evidence for an age-related defect in visual behavior. Brain Research 158, 456–460.CrossRefGoogle ScholarPubMed
Schwartz, M.L. & Goldman-Rakic, P.S. (1982). Single cortical neurones have axon collaterals to ipsilateral and contralateral cortex in fetal and adult primates. Nature 299, 154–155.CrossRefGoogle ScholarPubMed
Schwartz, M.L. & Rothblat, L.A. (1980). Long-lasting behavioral and dendritic spine deficits in the monocularly deprived albino rat. Experimental Neurology 68, 136–146.CrossRefGoogle ScholarPubMed
Sinnamon, H.M. & Galer, B.S. (1984). Head movements elicited by electrical stimulation of the anteromedial cortex of the rat. Physiology and Behavior 33, 185–190.CrossRefGoogle ScholarPubMed
Spear, P.D. & Barbas, H. (1975). Recovery of pattern discrimination ability in rats receiving serial or one-stage visual cortex lesions. Brain Research 94, 337–346.CrossRefGoogle ScholarPubMed
Sprague, J.M., Levy, J., Diberardino, A. & Berlucchi, G. (1977). Visual cortical areas mediating form discrimination in the cat. Journal of Comparative Neurology 172, 441–488.CrossRefGoogle ScholarPubMed
Steele Russell, I. & Pereira, S.C. (1981). Visual neglect in rat and monkey: an experimental model for the recovery of function following brain damage. In Functional Recovery from Brain Damage, ed. van Hof, M.W. & Mohn, G., pp. 209–238. Amsterdam: Elsevier.Google Scholar
Stein, D.G., Labbe, R., Atella, M.J. & Rakowsky, H.A. (1985). Fetal brain tissue transplants reduce visual deficits in adult rats with bilateral lesions of the occipital cortex. Behavioral and Neural Biology 44, 266–277.CrossRefGoogle ScholarPubMed
Stein, D.G. & Mufson, E.J. (1987). Morphological and behavioral characteristics of embryonic brain tissue transplants in adult, brain-damaged subjects. In Cell and Tissue Transplantation Into the Adult Brain, ed. Azmitia, E.G. & Bjorklund, A. pp. 444–463. New York: New York Academy of Sciences.Google Scholar
Steward, O. & Vinsant, S.L. (1978). Identification of the cells of origin of a central pathway which sprouts following lesions in mature rats. Brain Research 147, 223–243.CrossRefGoogle ScholarPubMed
Swanson, L.W. & Kohler, C. (1986). Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. Journal of Neuroscience 6, 3010–3023.CrossRefGoogle Scholar
Tees, R.C. (1984). Visual experience, unilateral cortical lesions, and lateralization of function in rats. Behavioral Neuroscience 98, 969–978.CrossRefGoogle ScholarPubMed
Vargo, J.M., Corwin, J.V., King, V. & Reep, R.L. (1987). Asymmetries in neglect and pattern of recovery following left vs right medial precentral prefrontal cortex lesions in rats. Society for Neuroscience Abstracts 13, 45.Google Scholar
Vogt, B.A. & Miller, M.W. (1981). Form and distribution of neurons in rat cingulate cortex: 32, 24, and 29. Journal of Comparative Neurology 195, 603–625.CrossRefGoogle Scholar
Vogt, B.A. & Miller, M.W. (1983). Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. Journal of Comparative Neurology 216, 192–210.CrossRefGoogle ScholarPubMed