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Fluoro-Gold tracing of zinc-containing afferent connections in the mouse visual cortices

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Summary

To identify zinc-containing projections to the visual areas, we injected Fluoro-Gold into the occipital cortex of the mouse. Five days later, the mice underwent an intravital selenium-labeling procedure to demonstrate the somata of neurons that give rise to zinc-containing boutons. Numerous double-labeled cells were seen in the ipsi- and contralateral primary (layers II/III and VI), and secondary visual cortices (layers II/III and VI). A few double-labeled cells were apparent in other cortical areas concerned with visual processing: the orbital cortex (layers II and III), the posterior portion of the medial agranular frontal cortex (layer V/VI border), and the temporal cortex (layer VI). The cingulate, retrosplenial, perirhinal, and lateral entorhinal cortices had lamina projecting to the visual cortex and separate lamina harboring zinc-containing cells. A spatial segregation of fluorescent and zinc-containing neurons was also seen in the claustrum. This integration or segregation of projecting and zinc-containing neurons may reflect the function of the cortical areas. N-methyl-d-aspartate receptor function is antagonized by physiological concentrations of zinc in vitro. It is proposed that zinc-positive projections from areas that perform basic visual functions are less likely to be modified by N-methyl-d-aspartate receptor-mediated processes than the zinc-negative connections from associational areas.

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References

  • Adams AD, Forrester JM (1968) The projection of the rat's visual field on the cerebral cortex. Q J Exp Physiol 53:327–336

    Google Scholar 

  • Artola A, Singer W (1987) Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330:649–652

    Google Scholar 

  • Bueno-López JL, Reblet C, López-Medina A, Gómez-Urquijo SM, Grandes P, Gondra J, Hennequet L (1991) Targets and laminar distribution of projection neurons with ‘inverted’ morphology in rabbit cortex. Eur J Neurosci 3:415–430

    Google Scholar 

  • Buisseret P, Gary-Bobo E, Milleret C (1988) Development of the kitten visual cortex depends on the relationship between the plane of eye movements and visual inputs. Exp Brain Res 72:83–94

    Google Scholar 

  • Burkhalter A, Charles V (1990) Organization of local axon collaterals of efferent projection neurons in rat visual cortex. J Comp Neurol 302:920–934

    Google Scholar 

  • Carey RG, Neal TL (1985) The rat claustrum: afferent and efferent connections with visual cortex. Brain Res 329:185–193

    Google Scholar 

  • Carey RG, Neal TL (1986) Reciprocal connections between the claustrum and visual thalamus in the tree shrew (Tupaia glis). Brain Res 386:155–168

    Google Scholar 

  • Carey RG, Rieck RW (1987) Topographic projections to the visual cortex from the basal forebrain in the rat. Brain Res 424:205–215

    Google Scholar 

  • Caviness Jr VS (1975) Architectonic map of neocortex of the normal mouse. J Comp Neurol 164:247–264

    Google Scholar 

  • Caviness Jr VS, Frost DO (1980) Tangential organization of thalamic projections to the neocortex in the mouse. J Comp Neurol 94:335–367

    Google Scholar 

  • Cortimiglia R, Crescimanno G, Salerno MT, Amato G (1991) The role of the claustrum in the bilateral control of frontal oculomotor neurons in the cat. Exp Brain Res 84:471–477

    Google Scholar 

  • Cotman CW, Monaghan DT, Ottersen OP, Storm-Mathisen J (1987) Anatomical organization of excitatory amino acid receptors and their pathways. TINS 10:273–280

    Google Scholar 

  • Crowne DP, Pathria MN (1982) Some attentional effects of unilateral frontal lesions in the rat. Behav Brain Res 6:25–39

    Google Scholar 

  • Danscher G (1981) Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electronmicroscopy. Histochemistry 71:1–16

    Google Scholar 

  • Danscher G (1982) Exogenous selenium in the brain. Histochemistry 76:281–293

    Google Scholar 

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

    Google Scholar 

  • Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88

    Google Scholar 

  • Doyon J, Milner B (1991) Right temporal-lobe contribution to global visual processing. Neuropsychologia 29:343–360

    Google Scholar 

  • Dräger UC, Hubel DH (1975) Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. J Neurophysiol 38:690–713

    Google Scholar 

  • Garrett B, Geneser FA, Slomianka L (1991) Distribution of acetylcholinesterase and zinc in the visual cortex of the mouse. Anat Embryol 184:461–468

    Google Scholar 

  • Gochin PM, Miller EK, Gross CG, Gerstein GL (1991) Functional interactions among neurons in inferior temporal cortex of the awake macaque. Exp Brain Res 84:505–516

    Google Scholar 

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

    Google Scholar 

  • Hess BJM, Precht W, Reber A, Cazin L (1985) Horizontal optokinetic ocular nystagmus in the pigmented rat. Neuroscience 15:97–107

    Google Scholar 

  • Jones KA, Baughman RW (1988) NMDA- and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. J Neurosci 8:3522–3534

    Google Scholar 

  • Katz LC (1987) Local circuitry of identified projection neurons in cat visual cortex brain slices. J Neurosci 7:1223–1249

    Google Scholar 

  • Keating EG, Gooley SG (1988) Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures. Brain Res 438:247–255

    Google Scholar 

  • Keller EL, Heinen SJ (1991) Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways. Neurosci Res 11:79–107

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Baldwin BA (1989) Visual responses of sheep temporal cortex cells to moving and stationary human images. Neurosci Lett 100:193–197

    Google Scholar 

  • Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157–192

    Google Scholar 

  • Krieg WJS (1946) Connections of the cerebral cortex. J Comp Neurol 84:221–323

    Google Scholar 

  • Krubitzer LA, Kaas JH (1989) Cortical integration of parallel pathways in the visual system of primates. Brain Res 478:161–165

    Google Scholar 

  • LeVay S, Sherk H (1981) The visual claustrum of the cat. I. Structure and connections. J Neurosci 1:956–980

    Google Scholar 

  • Macchi G, Bentivoglio M, Minciacchi D, Molinari M (1983) Claustroneocortical projections studied in the cat by means of multiple retrograde fluorescent tracing. J Comp Neurol 215:121–134

    Google Scholar 

  • Maragos WF, Penney JB, Young AB (1988) Anatomic correlation of NMDA and 3H-TCP-labeled receptors in rat brain. J Neurosci 8:493–501

    Google Scholar 

  • Mignard M, Malpeli JG (1991) Paths of information flow through visual cortex. Science 251:1249–1251

    Google Scholar 

  • Miller MW (1988) Maturation of rat visual cortex: IV. The generation, migration, morphogenesis, and connectivity of atypically oriented pyramidal neurons. J Comp Neurol 274:387–405

    Google Scholar 

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

    Google Scholar 

  • Minciacchi D, Molinari M, Bentivoglio M, Macchi G (1985) The organization of the ipsi-and contralateral claustrocortical system in rat with notes on the bilateral claustrocortical projections in cat. Neuroscience 16:557–576

    Google Scholar 

  • Müller-Paschinger I-B, Tömböl T (1989) Cortico-cortical and subcortico-cortical afferent connections of the rabbit's primary visual cortex. Anat Embryol 180:81–88

    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, Mignano LR, Van Sluyters RC (1982) Pattern of extrastriate visual areas connecting reciprocally with striate cortex in the mouse. Exp Neurol 78:775–779

    Google Scholar 

  • Paperna T, Malach R (1991) Patterns of sensory intermodality relationships in the cerebral cortex of the rat. J Comp Neurol 308:432–456

    Google Scholar 

  • Parnavelas JG, Lieberman AR, Webster KE (1977) Organization of neurons in the visual cortex, area 17, of the rat. J Anat 124:305–322

    Google Scholar 

  • Rauschecker JP (1991) Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. Physiol Rev 71:587–614

    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 

  • Salerno MT, Cortimiglia R, Crescimanno G, Amato G (1989) Effect of claustrum activation on the spontaneous unitary activity of frontal eye field neurons in the cat. Neurosci Lett 98:299–304

    Google Scholar 

  • Saper CB (1984) Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J Comp Neurol 222:313–342

    Google Scholar 

  • Sawchenko PE, Swanson LW (1981) A method for tracing biochemically defined pathways in the central nervous system using combined fluorescence retorgrade transport and immunohistochemical techniques. Brain Res 210:31–51

    Google Scholar 

  • Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147–154

    Google Scholar 

  • Sefton AJ, Dreher B, Lim W-L (1991) Interactions between callosal, thalamic and associational projections to the visual cortex of the developing rat. Exp Brain Res 84:142–158

    Google Scholar 

  • Sidman RL, Angevine Jr JB, Pierce ET (1971) Atlas of the Mouse Brain and Spinal Cord. Harvard University Press, Cambridge, Mass

    Google Scholar 

  • Simmons PA, Lemmon V, Pearlman AL (1982) Afferent and efferent connections of the striate and extrastriate visual cortex of the normal and reeler mouse. J Comp Neurol 211:295–308

    Google Scholar 

  • Slomianka L, Danscher G, Frederickson CJ (1990) Labeling of the neurons of origin of zinc-containing pathways by intraperitoneal injections of sodium selenite. Neuroscience 38:843–854

    Google Scholar 

  • Sukekawa K (1988) Interconnections of the visual cortex with the frontal cortex in the rat. J Hirnforsch 29:83–93

    Google Scholar 

  • Swanson LW, Köhler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010–3023

    Google Scholar 

  • Tanaka K, Saito H-A, Fukada Y, Moriya M (1991) Coding visual images of objects in the inferotemporal cortex of the macaque monkey. J Neurophysiol 66:170–189

    Google Scholar 

  • Teyler T, Aroniadou V, Berry RL, Borroni A, DiScenna P, Grower L, Lambert N (1990) LTP in neocortex. Seminars Neurosci 2:265–279

    Google Scholar 

  • Thurlow GA, Cooper RM (1988) Metabolic activity in striate and extrastriate cortex in the hooded rat: contralateral and ipsilateral eye input. J Comp Neurol 274:595–607

    Google Scholar 

  • Tsumoto T (1990) Long-term potentiation and depression in the cerebral neocortex. Jpn J Physiol 40:573–593

    Google Scholar 

  • Van Groen T, Wyss JM (1990) Connections of the retrosplenial granular A cortex in the rat. J Comp Neurol 300:593–606

    Google Scholar 

  • Vaudano E, Legg CR, Glickstein M (1991) Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur J Neurosci 3:317–330

    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 

  • Wong EHF, Kemp JA (1991) Sites for antagonism on the N-methyl-d-aspartate receptor channel complex. Annu Rev Pharmacol Toxicol 31:401–25

    Google Scholar 

  • Woodward WR, Coull BM (1988) Effects of kainic acid lesions in lateral geniculate nucleus: activity dependence of retrograde axonal transport of fluorescent dyes. Brain Res 454:106–115

    Google Scholar 

  • Wree A, Zilles K, Schleicher Z (1983) A quantitative approach to cytoarchitectonics VIII. The areal pattern of the cortex of the albino mouse. Anat Embryol 166:333–353

    Google Scholar 

  • Zilles K (1985) The Cortex of the Rat. Springer, Berlin

    Google Scholar 

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Authors and Affiliations

  1. Department of Neurobiology, Institute of Anatomy, University of Aarhus, DK-8000, Aarhus C, Denmark

    B. Garrett, J. C. Sørensen & L. Slomianka

  2. Stereological Research Laboratory, University of Aarhus, DK-8000, Aarhus C, Denmark

    L. Slomianka

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  1. B. Garrett
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  2. J. C. Sørensen
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  3. L. Slomianka
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Garrett, B., Sørensen, J.C. & Slomianka, L. Fluoro-Gold tracing of zinc-containing afferent connections in the mouse visual cortices. Anat Embryol 185, 451–459 (1992). https://doi.org/10.1007/BF00174083

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