Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T03:51:15.937Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental changes in the pattern of NADPH-diaphorase staining in the cat's lateral geniculate nucleus

Published online by Cambridge University Press:  02 June 2009

William Guido ,
Christopher A. Scheiner ,
R. Ranney Mize  and
Kenneth E. Kratz
William Guido
Affiliation:
Department of Anatomy and Neuroscience Center of Excellence, LSU Medical Center, New Orleans
Christopher A. Scheiner
Affiliation:
Department of Anatomy and Neuroscience Center of Excellence, LSU Medical Center, New Orleans
R. Ranney Mize
Affiliation:
Department of Anatomy and Neuroscience Center of Excellence, LSU Medical Center, New Orleans
Kenneth E. Kratz
Affiliation:
Department of Anatomy and Neuroscience Center of Excellence, LSU Medical Center, New Orleans
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined the pattern of NADPH-diaphorase (NADPH-d) staining in the lateral geniculate nucleus (LGN) of dorsal thalamus in fetal and newborn kittens, and adult cats. This staining visualizes the synthesizing enzyme of nitric oxide (NO), a neuromodulator associated with central nervous system (CNS) development and synaptic plasticity. In the adult, very few LGN cells stained for NADPH-d, and these were restricted to interlaminar zones and ventral C layers. NADPH-d labeled a dense network of fibers and axon terminals throughout the LGN and adjacent thalamic nuclei. The source of such labelling has been reported to be cholinergic neurons from the parabrachial region of the brain stem (Bickford et al., 1993). A very different pattern of staining was observed in prenatal and early postnatal kittens. Between embryonic (E) day 46–57, lightly stained cells appeared throughout the LGN. From this age, through about the first month of life, the number of stained cells in the LGN rose rapidly. The density (cells/ mm2) of labeled cells peaked at postnatal day (P) 28 (P28), and was about 150 times greater than the level measured in the adult LGN. After P28, cell staining declined rapidly, and fell to adult levels at P41. The reduction in cell staining that occurred between P35–41 was accompanied by the appearance of fine-caliber fiber staining, similar to that observed in the adult LGN. NADPH-d staining, which reveals the presence of nitric oxide synthase (NOS), and thus NO activity, may reflect two processes. In the adult LGN, the labeling of cholinergic axons arising from the brain-stem parabrachial region coupled with a paucity of the LGN cellular staining suggests that NO operates in an orthograde manner, being co-released with ACh to influence the gain and efficacy of retinogeniculate transmission. By contrast, in developing kitten, NADPH-d staining of LGN cells suggests that NO acts in a retrograde fashion, perhaps playing a role in maintaining associative processes underlying activity-dependent refinement of retinogeniculate connections.

Keywords

Nitric oxidePlasticityDevelopmentRetinogeniculate pathwaySynaptic transmission
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1167 - 1173
Copyright
Copyright © Cambridge University Press 1997

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

Banfro, F. & Mize, R.R. (1996). The clustered cell system is present before the formation of the Ach patches in the intermediate gray layer of the cat superior colliculus. Brain Research 733, 273–283.CrossRefGoogle ScholarPubMed
Bear, M.F. & Abraham, W.C. (1996). Long-term depression in hippocampus. Annual Review of Neuroscience 19, 437–462.CrossRefGoogle ScholarPubMed
Bear, M.F. & Malenka, R.C. (1994). Synaptic plasticity, LTP and LTD. Current Opinions in Neurobiology 4, 389–399.CrossRefGoogle ScholarPubMed
Bickford, M.E., Günlük, A.E., Guido, W. & Sherman, S.M. (1993). Evidence that cholinergic axons from the parabrachial region of the brainstem are the exclusive source of nitric oxide in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 334, 410–430.CrossRefGoogle ScholarPubMed
Bredt, D.S., Glatt, C.E., Hwang, P.M., Fotuhi, M., Dawson, T.M. & Snyder, S.H. (1991). Nitric oxide synthase protein & MRNA are discretely localized in neuronal populations of mammalian CNS together with NADPH-d diaphorase. Neuron 7, 615–624.CrossRefGoogle Scholar
Constantine-Paton, M., Cline, H.T. & Debski, E. (1990). Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Review of Neuroscience 13, 129–154.CrossRefGoogle ScholarPubMed
Cramer, K.S., Angelucci, A., Hahm, J.-O., Bogdanov, M. & Sur, M. (1996). A role for nitric oxide in the developing ferret retinogeniculate projection. Journal of Neuroscience 16, 7995–8004.CrossRefGoogle ScholarPubMed
Cramer, K.S., Moore, C.I. & Sur, M. (1995). Transient expression of NADPH-d-Diaphorase in the lateral geniculate nucleus of the ferret during early postnatal development. Journal of Comparative Neurology 353, 306–315.CrossRefGoogle ScholarPubMed
Cramer, K.S. & Sur, M. (1995). Activity dependent remodeling of connections in the mammalian visual system. Current Opinion in Neurobiology 5, 106–111.CrossRefGoogle ScholarPubMed
Cudeiro, J., Grieve, K.L., Rivadulla, C., Rodriguez, R., Martinez-Conde, S. & Acuna, C. (1994 a). The role of nitric oxide in the transformation of visual information within the dorsal lateral geniculate nucleus of the cat. Neuropharmacology 11, 1413–1418.CrossRefGoogle Scholar
Cudeiro, J., Rivadulla, C., Rodriguez, R., Martinez-Conde, S., Acuna, C. & Alonso, J.M. (1994 b). Modulatory influence of putative inhibitors of nitric oxide synthesis on visual processing in the cat lateral geniculate nucleus. Journal of Neurophysiology 71, 146–149.CrossRefGoogle ScholarPubMed
Cudeiro, J., Rivadulla, C., Rodriguez, R., Martinez-Conde, S., Grieve, K.L. & Acuna, C. (1996). Further observations on the role of nitric oxide in the feline lateral geniculate nucleus. European Journal of Neuroscience 8, 144–152.CrossRefGoogle ScholarPubMed
Dalva, M.B., Ghosh, A. & Shatz, C.J. (1994). Independent control of dendritic and axonal form in the developing lateral geniculate nucleus. Journal of Neuroscience 14, 3588–3602.Google ScholarPubMed
Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. & Synder, S.H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academy of Sciences of the U.S.A. 88, 7797–7801.CrossRefGoogle ScholarPubMed
Dubin, M.W., Stark, L.A. & Archer, S.M. (1986). A role for actionpotential activity in the development of neuronal connections in the kitten retinogeniculate pathway. Journal of Neuroscience 6, 1021–1036.CrossRefGoogle ScholarPubMed
Erişir, A., Van Horn, S.C., Bickford, M.E. & Sherman, S.M. (1997). Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: A comparison with corticogeniculate terminals. Journal of Comparative Neurology 377, 535–544.Google Scholar
Garraghty, P.E. & Sur, M. (1993). Competitive interactions influencing the development of retinal axonal arbors in the cat lateral geniculate nucleus. Physiological Reviews 73, 529–545.CrossRefGoogle ScholarPubMed
Goodman, C.S. & Shatz, C.J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72, 77–98.CrossRefGoogle ScholarPubMed
Günlük, A.E., Bickford, M.E. & Sherman, S.M. (1994). Rearing with monocular lid suture induces abnormal NADPH-d-diaphorase staining in the lateral geniculate nucleus of cats. Journal of Comparative Neurology 350, 215–228.CrossRefGoogle ScholarPubMed
Hahm, J.-O., Langdon, R.B. & Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 568–570.CrossRefGoogle ScholarPubMed
Hope, B.T., Micheal, G.J., Knigge, K.M. & Vincent, S.R. (1991). Neuronal NADPH diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2811–2814.CrossRefGoogle ScholarPubMed
Mooney, R., Madison, D.V. & Shatz, C.J. (1993). Enhancement of transmission at the developing retinogeniculate synapse. Neuron 10, 815–825.CrossRefGoogle ScholarPubMed
Mothet, J.P., Fossier, P., Tauc, L. & Baux, G. (1996). NO decreases evoked quantal Ach release at a synapse of Aplysia by a mechanism independent of Ca2+ influx and protein kinase. Journal of Physiology 493.3, 769–784.CrossRefGoogle Scholar
Pape, H.-C. & Mager, R. (1992). Nitric oxide controls oscillatory activity in thalamocortical neurons. Neuron 9, 441–448.CrossRefGoogle ScholarPubMed
Ramoa, A.S. & McCormick, D.A. (1994). Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse. Journal of Neuroscience 14, 2098–2105.CrossRefGoogle ScholarPubMed
Rocha, M. & Sur, M. (1995). Rapid acquisition of dendritic spine by visual thalamic neurons after blockade of NMDA receptors. Proceedings of the National Academy of Sciences of the U.S.A. 92, 8026–8030.CrossRefGoogle Scholar
Scharfman, H.E., Lu, S.M., Guido, W., Adams, P.R. & Sherman, S.M. (1990). N-methyI-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proceedings of the National Academy of Sciences of the U.S.A. 87, 4548–4552.CrossRefGoogle Scholar
Schuman, E.M. & Madison, D.V. (1994). Nitric oxide and synaptic function. Annual Review of Neuroscience 17, 153–183.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1990 a). Competitive interactions between retinal ganglion cells during prenatal development. Journal of Neurobiology 21, 197–211.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1990 b). Impulse activity and the patterning of connections during CNS development. Neuron 5, 745–756.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1996). Emergence of order in visual system development. Proceedings of the National Academy of Sciences of the U.S.A. 93, 602–608.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Sretavan, D.W. (1986). Interactions between retinal ganglion cells during the development of the mammalian visual system. Annual Review of Neuroscience 9, 171–207.CrossRefGoogle ScholarPubMed
Sherman, S.M. (1985). Functional organization of the W-, X-, and Y-cell pathways, a review and hypothesis. In Progress in Psychobiology and Physiological Psychology, Vol. II, ed. Sprague, J.M. & Epstein, A.N., pp. 233–314. New York: Academic Press.Google Scholar
Sherman, S.M. & Spear, P.D. (1982). Organization of the visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738–855.CrossRefGoogle ScholarPubMed
Sur, M. (1988). Development and plasticity of retinal X and Y axon terminations in the cat's lateral geniculate nucleus. Brain, Behavior, and Evolution 31, 243–251.CrossRefGoogle ScholarPubMed
Vincent, S.R. & Kimura, H. (1992). Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46, 755–784.CrossRefGoogle ScholarPubMed
Williams, C.V., Nordquist, D. & McCloon, S.C. (1994). Correlation of nitric oxide synthase expression with the changing patterns of axonal projection in the developing visual system. Journal of Neuroscience 14, 1746–1755.CrossRefGoogle ScholarPubMed
Williams, J.A., Vincent, S.R., & Reiner, P.B. (1997). Nitric oxide production in rat thalamus changes with behavioral state, local depolarization, and brainstem stimulation. Journal of Neuroscience 17, 420–427.CrossRefGoogle ScholarPubMed
Wu, H.H., Waid, D.K. & McCloon, S.C. (1996). Nitric oxide and the developmental remodeling of retinal connections in the brain. Progress in Brain Research 108, 1593–1596.Google ScholarPubMed
Wu, H.H., Williams, C.V. & McCloon, S.C. (1994). Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science 265, 1593–1596.CrossRefGoogle ScholarPubMed