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Interactions between callosal, thalamic and associational projections to the visual cortex of the developing rat

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The patterns of callosal interconnections between the visual cortices of rats display considerable plasticity in response to various neonatal manipulations. In the present study, many neurones in the principal visual thalamic relay nuclei, the dorsal lateral geniculate nucleus (DLG) and to a lesser extent those in the lateral posterior nucleus (LP) were destroyed by injections of the neurotoxin — kainic acid — on the first day of postnatal life. Four weeks later, as demonstrated with the anterograde and retrograde transport of the enzyme horseradish peroxidase (HRP) injected into the occipital lobe of one hemisphere, callosally projecting neurones and terminals were distributed more widely in the retinotopically organized areas 17, 18a and 18b of the visual cortex ipsilateral to the lesioned visual thalamus than in unoperated control animals of the same age. By contrast, in the visual cortex contralateral to the lesioned visual thalamus the areal distribution of callosally projecting neurones and terminals was similar to that of the controls, that is, largely but not exclusively restricted to the common border of areas 17 and 18a. Both in unoperated and operated animals, cells in lamina V of several cytoarchitectonically defined areas that are not retinotopically organized (area 8 in the frontal lobe, area 29d in the retrosplenial limbic cortex and perirhinal areas 35/13 in the temporal lobe) also project to contralateral visual cortices. In areas 8 and 29d, the total numbers, laminar distributions and densities of labelled callosal cells both ipsilateral and contralateral to the kainate-injected visual thalamus were similar to those in the controls. However, in the temporal lobe, the areal distribution of the labelled callosal neurones was more extensive than that in the controls and labelled cells in areas 35/13 of the cortex contralateral to the kainate-lesioned visual thalamus merged with those in the neighbouring areas 20 and 36. By contrast, the areal distribution of associational neurones in area 18a and in nonretinotopically organized areas projecting to area 17 were very similar in controls and in operated animals (neonatal kainate lesion of the visual thalamus, neonatal section of the corpus callosum or both procedures combined). However, in operated animals, the labelled associational neurones projecting from the supragranular laminae (II/III) of area 18a to area 17 constituted a higher proportion of all cells than did those in the unoperated control animals. Thus, overall the number of associational neurones projecting from area 18a to area 17 was slightly increased by the experimental manipulations performed. The implications of these results concerning the mechanism(s) underlying the developmental changes in the distribution of commissural and associational neurones projecting to the rat's visual cortex are discussed.

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References

  • Bruce LL, Stein BE (1988) Transient projections from the lateral geniculate to the posteromedial lateral suprasylvian visual cortex in kittens. J Comp Neurol 278:287–302

    Google Scholar 

  • Bullier J, Dehay C, Dreher B (1990) Bihemispheric axonal bifurcation of the afferents to the visual cortical areas during postnatal development in the rat. Europ J Neurosci 2:332–343

    Google Scholar 

  • Burkhalter A (1989) Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. J Comp Neurol 279:171–186

    Google Scholar 

  • Carpenter P, Sefton AJ, Dreher B, Lim W-L (1986) Role of target tissue in regulating the development of retinal ganglion cells in the albino rat: effects of kainate lesions in the superior colliculus. J Comp Neurol 251:240–259

    Google Scholar 

  • Chow KL, Baumbach HD, Lawson R (1981) Callosal projections of the striate cortex in the neonatal rabbit. Exp Brain Res 42:122–126

    Google Scholar 

  • Coleman J, Clerici WJ (1980) Extrastriate projections from thalamus to posterior occipitotemporal cortex in rat. Brain Res 194:205–209

    Google Scholar 

  • Coogan TA, Burkhalter A (1988) Sequential development of connections between striate and extrastriate visual cortical areas in the rat. J Comp Neurol 278:242–252

    Google Scholar 

  • Cusick CG, Lund RD (1982) Modification of visual callosal projections in rats. J Comp Neurol 212:385–398

    Google Scholar 

  • Deacon TW, Eichenbaum H, Rosenberg P, Eckmann RW (1983) Afferent connections of the perirhinal cortex in the rat. J Comp Neurol 220:168–190

    Google Scholar 

  • Dehay C, Kennedy H, Bullier J (1988) Characterization of transient cortical projections from auditory, somatosensory and motor cortices to visual areas 17, 18 and 19 in the kitten. J Comp Neurol 272:68–89

    Google Scholar 

  • Dreher B, Dehay C, Bullier J (1990) Bihemispheric collateralization of the cortical and subcortical afferents to the rat's visual cortex. Europ J Neurosci 2:317–331

    Google Scholar 

  • Dreher B, Thong IG, Shameem N, McCall MJ (1985) Development of cortical afferents and cortico-tectal efferents of the mammalian (rat) primary visual cortex. Aust NZ J Ophthalmol 13:251–261

    Google Scholar 

  • Fish SE, Mooney RD, Rhoades RW (1985) Development and plasticity of mammalian striate corticofugal pathways. In: Aslin RN (ed) Advances in neural and behavioral development, Vol I. Ablex Publishing Corporation, Norwood NJ, pp 157–186

    Google Scholar 

  • Galli L, Maffei L (1988) Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242:90–91

    Google Scholar 

  • Granger EM, Masterton RB, Glendenning KK (1985) Origin of interhemispheric fibers in acallosal opossum (with a comparison to callosal origins in rat). J Comp Neurol 241:82–98

    Google Scholar 

  • Halasz P, Martin PR (1984) A microcomputer based system for the semi-automatic analysis of histological sections. Proc R Microsc Soc 11:312P

  • Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23–38

    Google Scholar 

  • Hallman LC, Schofield BR, Lin C-S (1988) Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurones in layer V of primary visual cortex of the hooded rat. J Comp Neurol 272:149–160

    Google Scholar 

  • Horsburgh GM, Sefton AJ (1987) Cellular degeneration and synaptogenesis in the developing retina of the rat. J Comp Neurol 263:553–566

    Google Scholar 

  • Hsiao R, Sachs GM, Schneider GE (1984) A minute fraction of Syrian golden hamster retinal ganglion cells project bilaterally. J Neurosci 4:359–367

    Google Scholar 

  • Hughes H (1977) Anatomical and neurobehavioral investigations concerning the thalamocortical organization of the rat's visual system. J Comp Neurol 175:311–336

    Google Scholar 

  • Innocenti GM (1986) General organization of callosal connections in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex, Vol V. Plenum Publishing Corporation, New York, pp 291–353

    Google Scholar 

  • Innocenti GM, Clarke S (1986) Organization of immature intrahemispheric connections. J Comp Neurol 251:1–22

    Google Scholar 

  • Innocenti GM, Clarke S, Kraftsik R (1986) Interchange of callosal and association projections in the developing visual cortex. J Neurosci 6:1384–1409

    Google Scholar 

  • Jacobson S (1970) Distribution of commissural axon terminals in the rat neocortex. Exp Neurol 28:193–205

    Google Scholar 

  • Jacobson S, Trojanowski J (1974) The cells of origin of the corpus callosum in rat, cat and rhesus monkey. Brain Res 74:149–155

    Google Scholar 

  • Jeffery G (1984) Transneuronal effects of early eye removal on geniculo-cortical projection cells. Dev Brain Res 13:257–263

    Google Scholar 

  • Jones EG (1985) The thalamus. Plenum Publishing Corporation, New York

    Google Scholar 

  • Keefer DA (1978) Horseradish peroxidase as a retrogradely-transported detailed dendritic marker. Brain Res 140:15–32

    CAS  Google Scholar 

  • Kennedy H, Bullier J, Dehay C (1989) Transient projections from the superior temporal sulcus to area 17 in the newborn macaque monkey. Proc Natl Acad Sci USA 86:8093–8097

    Google Scholar 

  • Land PW, Lund RD (1979) Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science 205:698–700

    Google Scholar 

  • Lent R (1983) Cortico-cortical connections reorganize in hamsters after neonatal transection of the callosal bridge. Dev Brain Res 11:137–142

    Google Scholar 

  • Lent R (1984) Neuroanatomical effects of neonatal transection of the corpus callosum in hamsters. J Comp Neurol 223:548–555

    Google Scholar 

  • Lim W-L, Dreher B, Sefton AJ (1986) Callosal connections in the mature rat visual cortex after neonatal selective lesions of the lateral geniculate nucleus. Neurosci Lett Suppl 23:S62

    Google Scholar 

  • Lund JS (1988) Anatomical organization of macaque monkey striate visual cortex. Ann Rev Neurosci 11:253–288

    Google Scholar 

  • Lund JS, Lund RD (1970) The termination of callosal fibers in the paravisual cortex of the rat. Brain Res 17:25–45

    Google Scholar 

  • Lund RD, Mustari MJ (1977) Development of the geniculocortical pathway in rats. J Comp Neurol 173:289–306

    Google Scholar 

  • Lund RD, Chang F-LF, Land PW (1984) The development of callosal projections in normal and one-eyed rats. Dev Brain Res 14:139–142

    Google Scholar 

  • Mastronarde DN (1989) Correlated firing of retinal ganglion cells. Trends Neurosci 12:75–80

    Google Scholar 

  • Mesulam M-M (1982) Tracing neuronal connections with horseradish peroxidase. In: Smith AD (ed) IBRO handbook series: methods in neuroscience. Wiley, Chichester, pp 251

    Google Scholar 

  • Miller MW, Vogt BA (1984a) Heterotopic and homotopic callosal connections in rat visual cortex. Brain Res 297:75–89

    Google Scholar 

  • Miller MW, Vogt BA (1984b) The postnatal growth of the callosal connections of primary and secondary visual cortex in the rat. Dev Brain Res 14:304–309

    Google Scholar 

  • Miller MW, Vogt BA (1984c) Direct connections of rat visual cortex with sensory, motor and association cortex. J Comp Neurol 226:184–202

    Google Scholar 

  • Montero VM (1981) Comparative studies of the visual cortex. In: Woolsey CN (ed) Cortical sensory organization, Vol. 2. Multiple visual areas. Humana Press, Clifton NJ, pp 33–82

    Google Scholar 

  • Montero VM, Rojas A, Torrealba F (1973) Retinotopic organization of striate and peristriate visual cortex in the albino rat. Brain Res 53:197–201

    Google Scholar 

  • Mooney RD, Rhoades RW, Fish SE (1984) Neonatal superior collicular lesions alter visual callosal development in hamster. Exp Brain Res 55:9–25

    Google Scholar 

  • Nauta WJH, Bucher VM (1954) Efferent connections of the striate cortex in the albino rat. J Comp Neurol 100:257–285

    Google Scholar 

  • Olavarria J, Montero VM (1981) Reciprocal connections between the striate cortex and extrastriate cortical visual areas in the rat. Brain Res 217:358–363

    Google Scholar 

  • Olavarria J, Montero VM (1984) Relation of callosal and striateextrastriate cortical connections in the rat: morphological definition of extrastriate visual areas. Exp Brain Res 54:240–252

    Google Scholar 

  • Olavarria J, Van Sluyters RC (1983) Widespread callosal connections in infragranular visual cortex of the rat. Brain Res 279:233–237

    Google Scholar 

  • Olavarria J, Van Sluyters RC (1984) Callosal connections of the posterior neocortex in normal-eyed, congenitally anophthalmic, and neonatally enucleated mice. J Comp Neurol 230:249–268

    Google Scholar 

  • Olavarria J, Van Sluyters RC (1985) Organization and postnatal development of callosal connections in the visual cortex of the rat. J Comp Neurol 239:1–26

    Google Scholar 

  • Olavarria J, Van Sluyters RC, Killackey HP (1984) Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res 291:364–368

    Google Scholar 

  • Olavarria J, Malach R, Van Sluyters RC (1987) Development of visual callosal connections in neonatally enucleated rats. J Comp Neurol 260:321–348

    Google Scholar 

  • Olavarria J, Serra-Oller MM, Yee KT, Van Sluyters RC (1988) Topography of interhemispheric connections in neocortex of mice with congenital deficiencies of the callosal commissure. J Comp Neurol 270:575–590

    Google Scholar 

  • O'Leary DDM, Fricke RA, Stanfield BB, Cowan WM (1979) Changes in the associational afferents to the dentate gyrus in the absence of its commissural input. Anat Embryol 156: 268–299

    Google Scholar 

  • O'Leary DDM, Stanfield BB, Cowan WM (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. Dev Brain Res 1:607–617

    Google Scholar 

  • Ozaki HS, Iwahashi K, Shimada M (1989) Ipsilateral corticocortical projections of fibers which course within Probst's longitudinal bundle seen in the brains of mice with congenital absence of the corpus callosum: a study with the horseradish peroxidase technique. Brain Res 493:66–73

    Google Scholar 

  • Parnavelas JG, McDonald JK (1983) The cerebral cortex. In: Emson PC (ed) Chemical neuroanatomy. Raven, New York, pp 505–549

    Google Scholar 

  • Price DJ, Blakemore C (1985) Regressive events in the postnatal development of associational projections in the visual cortex. Nature 316:721–724

    Google Scholar 

  • Rhoades RW, Fish SE (1983) Bilateral enucleation alters visual callosal but not corticotectal or corticogeniculate projections in hamster. Exp Brain Res 51:451–462

    Google Scholar 

  • Rhoades RW, Mooney RD, Fish SE (1984) A comparison of visual callosal organization in normal, bilaterally enucleated and congenitally anophthalmic mice. Exp Brain Res 56:92–105

    Google Scholar 

  • Rhoades RW, Fish SE, Mooney RD, Chiaia NL (1987) Distribution of visual callosal projection neurons in hamsters subjected to transection of the optic radiations on the day of birth. Dev Brain Res 32:217–232

    Google Scholar 

  • Ribak CE (1977) A note on the laminar organization of rat visual cortical projections. Exp Brain Res 27:413–418

    Google Scholar 

  • Ribak CE, Peters A (1975) An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Res 92:341–368

    Google Scholar 

  • Robinson SR, Dreher B (1990) The visual pathways of eutherian mammals and marsupials develop according to a common timetable. Brain Behav Evol 36:177–195

    Google Scholar 

  • Rothblat LA, Hayes LL (1982) Age-related changes in the distribution of visual callosal neurones following monocular enucleation in the rat. Brain Res 246:146–149

    Google Scholar 

  • Schober W (1981) Efferente und afferente Verbindungen des Nucleus lateralis posterior thalami (“Pulvinar”) der Albinoratte. Z Mikrosk Anat Forsch 95:827–844

    Google Scholar 

  • Schober W (1986) The rat cortex in stereotaxic coordinates. J Hirnforsch 27:121–143

    Google Scholar 

  • Schober W, Winkelmann E (1975) Der visuelle Kortex der Ratte: Cytoarchitektonik und stereotaktische Parameter. Z Mikrosk Anat Forsch 89:431–446

    Google Scholar 

  • Sefton AJ, Dreher B (1985) Visual system. In: Paxinos G (ed) The rat nervous system, Vol. 1. Academic Press, Sydney, pp 169–221

    Google Scholar 

  • Sefton AJ, Mackay-Sim A, Baur LA, Cottee LJ (1981) Cortical projections to visual centres in the rat: an HRP study. Brain Res 215:1–13

    Google Scholar 

  • Sefton AJ, Lim W-L, Dreher B (1986) Competition between geniculocortical and callosal afferents in the developing rat. Proc IUPS 30:P562.03

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw Hill Book Company, New York

    Google Scholar 

  • So K-F, Jen LS (1982) Visual callosal, corticotectal and corticogeniculate projections in golden hamsters. Brain Behav Evol 21:125–136

    MathSciNet  MATH  Google Scholar 

  • Thomas HC, Espinoza SG (1987) Relationships between interhemispheric cortical connections and visual areas in hooded rats. Brain Res 417:214–224

    Google Scholar 

  • Tracey DJ (1985) Somatosensory system. In: Paxinos G (ed) The rat nervous system, Vol. 2. Academic Press, Sydney, pp 129–152

    Google Scholar 

  • Vaughan DW, Foundas S (1982) Synaptic proliferation in the auditory cortex of young adult rat following callosal lesions. J Neurocytol 11:29–51

    Google Scholar 

  • Vaughan DW, Peters A (1985) Proliferation of thalamic afferents in cerebral cortex altered by callosal deafferentation. J Neurocytol 14:705–716

    Google Scholar 

  • Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:192–210

    Google Scholar 

  • Vogt BA, Peters A (1981) Form and distribution of neurones in rat cingulate cortex: areas 32, 24 and 29. J Comp Neurol 195:603–625

    Google Scholar 

  • Webster WR (1985) Auditory system. In: Paxinos G (ed) The rat nervous system, Vol. 2. Academic Press, Sydney, pp 153–184

    Google Scholar 

  • Windrem MS, Finlay BL (1985) Early thalamic lesions increase neonatal cell death and alter adult cytoarchitecture in the neocortex. Soc Neurosci Abstr 11:991

    Google Scholar 

  • Wise SP, Jones EG (1976) The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J Comp Neurol 168:313–344

    Google Scholar 

  • Wise SP, Jones EG (1978) Developmental studies of the thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 178:187–208

    Google Scholar 

  • Záborszky L, Wolff JR (1982) Distribution patterns and individual variations of callosal connections in the albino rat. Anat Embryol 165:213–272

    Google Scholar 

  • Zilles K, Wree A (1985) Cortex: areal and laminar structure. In: Paxinos G (ed) The rat nervous system, Vol. 1. Academic Press, Sydney, pp 375–415

    Google Scholar 

  • Zilles K, Zilles B, Schleicher A (1980) A quantitative approach to cytoarchitectonics. Anat Embryol 159:335–360

    Google Scholar 

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Sefton, A.J., Dreher, B. & Lim, WL. Interactions between callosal, thalamic and associational projections to the visual cortex of the developing rat. Exp Brain Res 84, 142–158 (1991). https://doi.org/10.1007/BF00231769

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