Home LiteratureArticle Details
PMID: 10627612 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity.

Wong WT, Myhr KL, Miller ED, Wong RO

Abstract

Synchronized spontaneous rhythmic activity is a feature common to many parts of the developing nervous system. In the early visual system, before vision, developing circuits in the retina generate synchronized patterns of bursting activity that contain information useful for patterning connections between retinal ganglion cells and their central targets. However, how developing retinal circuits generate and regulate these spontaneous activity patterns is still incompletely understood. Here we show that in developing retinal circuits, the nature of excitatory neurotransmission driving correlated bursting activity in ganglion cells is not fixed but undergoes a developmental shift from cholinergic to glutamatergic transmission. In addition, we show that this shift occurs as presynaptic glutamatergic bipolar cells form functional connections onto the ganglion cells, implicating the role of bipolar cells in providing endogenous drive to bursting activity later in development. This transition coincides with the period when subsets of ganglion cells (On and Off cells) develop distinct activity patterns that are thought to underlie the refinement of their connectivity with their central targets. Here, our results suggest that the differences in activity patterns of On and Off ganglion cells may be conferred by differential synaptic drive from On and Off bipolar cells, respectively. Taken together, our results suggest that the regulation of patterned spontaneous activity by neurotransmitters undergoes systematic change as new cellular elements are added to developing circuits and also that these new elements can help specify distinct activity patterns appropriate for shaping connectivity patterns at later ages.

MeSH Terms
2-Amino-5-phosphonovalerate/pharmacology Action Potentials/drug effects,physiology Animals Bicuculline/pharmacology Cholinergic Fibers/physiology Excitatory Amino Acid Antagonists/pharmacology Ferrets GABA Antagonists/pharmacology Glutamic Acid/metabolism Glycine/physiology Glycine Agents/pharmacology Interneurons/cytology,physiology Periodicity Quinoxalines/pharmacology Retina/cytology,growth & development,physiology Retinal Ganglion Cells/cytology,physiology Strychnine/pharmacology Synaptic Transmission/drug effects,physiology Vision, Ocular/physiology Visual Pathways gamma-Aminobutyric Acid/physiology
Chemicals
Excitatory Amino Acid Antagonists GABA Antagonists Glycine Agents Quinoxalines 2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline Glutamic Acid gamma-Aminobutyric Acid 2-Amino-5-phosphonovalerate Strychnine Glycine Bicuculline
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Wong W T
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Myhr K L
Miller E D
Wong R O
References (61)
61 references, click to expand
  1. Cholinergic regulation of [Ca2+]i during cell division and differentiation in the mammalian retina.
    J Neurosci. 1995 Apr;15(4):2696-706 PMID: 7722623
  2. Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells.
    Cell. 1994 May 6;77(3):361-9 PMID: 8181056
  3. Fast synaptic signaling by nicotinic acetylcholine and serotonin 5-HT3 receptors in developing visual cortex.
    J Neurosci. 1997 Nov 1;17(21):8353-62 PMID: 9334409
  4. Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact.
    J Neurosci. 1999 Apr 15;19(8):3007-22 PMID: 10191318
  5. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina.
    Science. 1991 May 17;252(5008):939-43 PMID: 2035024
  6. Rods and cones project to the inner plexiform layer during development.
    J Comp Neurol. 1999 Nov 8;414(1):1-12 PMID: 10494074
  7. 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research.
    Science. 1981 Jan 9;211(4478):182-5 PMID: 6255566
  8. A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb.
    J Neurosci. 1995 Apr;15(4):3075-83 PMID: 7722646
  9. The metabotropic glutamate agonist 2-amino-4-phosphonobutyric acid (APB) does not activate currents in postnatal retinal ganglion cells.
    Neuroreport. 1996 Nov 25;7(18):2873-7 PMID: 9116200
  10. Spontaneous calcium transients regulate neuronal plasticity in developing neurons.
    J Neurobiol. 1995 Mar;26(3):316-24 PMID: 7775965
  11. Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus.
    Neuron. 1997 Feb;18(2):243-55 PMID: 9052795
  12. Influence of spontaneous activity and visual experience on developing retinal receptive fields.
    Curr Biol. 1996 Nov 1;6(11):1503-8 PMID: 8939611
  13. Rod and cone pathways in the inner plexiform layer of cat retina.
    Science. 1974 Oct 4;186(4158):47-9 PMID: 4417736
  14. Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina.
    J Neurosci. 1996 Aug 15;16(16):5060-72 PMID: 8756436
  15. Morphological differentiation of bipolar cells in the ferret retina.
    Vis Neurosci. 1999 Nov-Dec;16(6):1133-44 PMID: 10614593
  16. Nicotinic modulation of [3H]dopamine release from striatal synaptosomes: pharmacological characterisation.
    J Neurochem. 1990 Mar;54(3):937-45 PMID: 2303820
  17. L-glutamate-induced responses and cGMP-activated channels in three subtypes of retinal bipolar cells dissociated from the cat.
    J Neurosci. 1995 May;15(5 Pt 1):3571-82 PMID: 7538564
  18. Responses to light of starburst amacrine cells.
    J Neurophysiol. 1996 Jan;75(1):469-80 PMID: 8822571
  19. Pattern formation by retinal afferents in the ferret lateral geniculate nucleus: developmental segregation and the role of N-methyl-D-aspartate receptors.
    J Comp Neurol. 1999 Aug 23;411(2):327-45 PMID: 10404257
  20. The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development.
    J Comp Neurol. 1981 Dec 1;203(2):189-211 PMID: 7309920
  21. Transient period of correlated bursting activity during development of the mammalian retina.
    Neuron. 1993 Nov;11(5):923-38 PMID: 8240814
  22. GABAA, NMDA and AMPA receptors: a developmentally regulated 'ménage à trois'.
    Trends Neurosci. 1997 Nov;20(11):523-9 PMID: 9364667
  23. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves.
    Science. 1996 May 24;272(5265):1182-7 PMID: 8638165
  24. Microcircuitry of bipolar cells in cat retina.
    J Neurosci. 1984 Dec;4(12):2920-38 PMID: 6502212
  25. Developmentally regulated spontaneous activity in the embryonic chick retina.
    J Neurosci. 1998 Nov 1;18(21):8839-52 PMID: 9786990
  26. Functional development of intrinsic properties in ganglion cells of the mammalian retina.
    J Neurophysiol. 1997 Dec;78(6):2895-903 PMID: 9405510
  27. Competition in retinogeniculate patterning driven by spontaneous activity.
    Science. 1998 Mar 27;279(5359):2108-12 PMID: 9516112
  28. Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina.
    Nature. 1993 Jul 8;364(6433):144-6 PMID: 8100613
  29. Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA.
    J Neurosci. 1998 May 15;18(10):3767-78 PMID: 9570807
  30. The acetylcholine receptor of the neuromuscular junction recognizes mecamylamine as a noncompetitive antagonist.
    Mol Pharmacol. 1985 Aug;28(2):128-37 PMID: 2410768
  31. Effects of glutamate and its analogs on intracellular calcium levels in the developing retina.
    Vis Neurosci. 1995 Sep-Oct;12(5):907-17 PMID: 8924414
  32. Maturation of function in the developing rabbit retina.
    J Comp Neurol. 1977 Oct 1;175(3):275-86 PMID: 903424
  33. Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina.
    J Neurosci. 1998 Jun 1;18(11):4155-65 PMID: 9592095
  34. Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity.
    J Neurosci. 1995 Nov;15(11):7037-45 PMID: 7472459
  35. Blockade of glutamate-mediated activity in the developing retina perturbs the functional segregation of ON and OFF pathways.
    J Neurosci. 1998 Jul 1;18(13):5019-25 PMID: 9634567
  36. Patterned neural activity in brain stem auditory areas of a prehearing mammal, the tammar wallaby (Macropus eugenii).
    Neuroreport. 1994 Feb 24;5(6):685-8 PMID: 8199338
  37. The mGluR6 5' upstream transgene sequence directs a cell-specific and developmentally regulated expression in retinal rod and ON-type cone bipolar cells.
    J Neurosci. 1997 May 1;17(9):3014-23 PMID: 9096137
  38. Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development.
    Neuron. 1996 Jun;16(6):1087-95 PMID: 8663985
  39. Retinal waves are governed by collective network properties.
    J Neurosci. 1999 May 1;19(9):3580-93 PMID: 10212317
  40. Blockade and recovery of spontaneous rhythmic activity after application of neurotransmitter antagonists to spinal networks of the chick embryo.
    J Neurosci. 1998 Jan 1;18(1):294-306 PMID: 9412508
  41. The origin of spontaneous activity in developing networks of the vertebrate nervous system.
    Curr Opin Neurobiol. 1999 Feb;9(1):94-104 PMID: 10072366
  42. Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: an immunocytochemical study.
    Vis Neurosci. 1994 Nov-Dec;11(6):1115-34 PMID: 7841121
  43. Spontaneous correlated activity in developing neural circuits.
    Neuron. 1999 Apr;22(4):653-6 PMID: 10230785
  44. Networks of coactive neurons in developing layer 1.
    Neuron. 1998 Mar;20(3):541-52 PMID: 9539127
  45. Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus.
    J Physiol. 1998 Feb 15;507 ( Pt 1):219-36 PMID: 9490842
  46. Retinal waves and visual system development.
    Annu Rev Neurosci. 1999;22:29-47 PMID: 10202531
  47. Synaptic activity and the construction of cortical circuits.
    Science. 1996 Nov 15;274(5290):1133-8 PMID: 8895456
  48. Histogenesis of the ferret retina.
    Exp Eye Res. 1981 Sep;33(3):315-32 PMID: 7286087
  49. Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity.
    J Neurosci. 2000 Jan 1;20(1):351-60 PMID: 10627612
  50. Retinal direction selectivity after targeted laser ablation of starburst amacrine cells.
    Nature. 1997 Sep 25;389(6649):378-82 PMID: 9311778
  51. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells.
    Nature. 1990 Jul 19;346(6281):269-71 PMID: 1695713
  52. Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors.
    Nature. 1991 Jun 13;351(6327):568-70 PMID: 1675433
  53. Dynamic processes shape spatiotemporal properties of retinal waves.
    Neuron. 1997 Aug;19(2):293-306 PMID: 9292720
  54. Blockade of afferent impulse activity disrupts on/off sublamination in the ferret lateral geniculate nucleus.
    Brain Res Dev Brain Res. 1997 Feb 20;98(2):287-90 PMID: 9051272
  55. Spontaneous activity in developing turtle retinal ganglion cells: pharmacological studies.
    J Neurosci. 1999 May 15;19(10):3874-87 PMID: 10234019
  56. Synaptic economics: competition and cooperation in synaptic plasticity.
    Neuron. 1996 Sep;17(3):371-4 PMID: 8816700
  57. Spontaneous Ca2+ transients and their transmission in the developing chick retina.
    Curr Biol. 1998 Feb 26;8(5):283-6 PMID: 9501073
  58. Model for the pharmacological basis of spontaneous synchronous activity in developing retinas.
    J Neurosci. 1994 Dec;14(12):7426-39 PMID: 7996185
  59. Evidence for glycine modulation of excitatory synaptic inputs to retinal ganglion cells.
    J Neurosci. 1995 Jun;15(6):4592-601 PMID: 7790926
  60. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life.
    Science. 1988 Oct 7;242(4875):90-1 PMID: 3175637
  61. Early functional neural networks in the developing retina.
    Nature. 1995 Apr 20;374(6524):716-8 PMID: 7715725
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2000-01-01
Pages
351-60
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6774128
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]