 |
Previous Article | Next Article 
Volume 17, Number 16,
Issue of August 15, 1997
pp. 6264-6276
Copyright ©1997 Society for Neuroscience
Temporal Correlations between Functional and Molecular Changes in
NMDA Receptors and GABA Neurotransmission in the Superior
Colliculus
Received March 26, 1997; revised May 16, 1997; accepted May 23, 1997.
Jian Shi,
Sandra M. Aamodt, and
Martha Constantine-Paton
Department of Biology, Yale University, New Haven, Connecticut
06520
Activation of the NMDA subtype of glutamate receptor is required
for activity-dependent structural plasticity in many areas of the young
brain. Previous work has shown that NMDA receptor currents decline
approximately at the time that developmental synaptic plasticity ends,
and in situ hybridization studies have suggested that
receptor subunit changes may be occurring during the same developmental
interval. To establish a system in which the relationship between these
properties of developing synapses can be explored, we have combined
patch-clamp recordings with mRNA- and protein-level biochemical
analyses to study the developmental regulation of NMDA receptors in the
superficial layers of the rat superior colliculus. These experiments
document an abrupt decrease in the NMDA receptor contribution to
synaptic currents that occurs before eye opening and is closely
associated with changes in NR1 protein, rapidly rising levels of the
NMDA receptor subunit NR2A, and decreasing levels of NR2B. The
functional and molecular changes also are correlated with the
developmental decline in structural plasticity in these layers. In
addition, both physiological and biochemical methods show evidence of
GABA-mediated inhibition in the superficial collicular layers beginning
after eye opening. This may provide an additional heterosynaptic
mechanism for controlling excitation and plasticity in this neuropil by
pattern vision. Thus our findings lend support to the idea that high
levels of NMDA receptor function are associated with the potential for
structural rearrangement in CNS neuropil and that the functional
downregulation of this molecule results, at least partially, from
changes in its subunit composition.
Key words:
NMDA receptors;
GABA;
activity-dependent;
superior
colliculus;
development;
downregulation
This article has been cited by other articles:

|
 |

|
 |
 
R. C. Ewald, K. R. Van Keuren-Jensen, C. D. Aizenman, and H. T. Cline
Roles of NR2A and NR2B in the Development of Dendritic Arbor Morphology In Vivo
J. Neurosci.,
January 23, 2008;
28(4):
850 - 861.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. J. Hall, B. Ripley, and A. Ghosh
NR2B Signaling Regulates the Development of Synaptic AMPA Receptor Current
J. Neurosci.,
December 5, 2007;
27(49):
13446 - 13456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Groc, D. Choquet, F. A. Stephenson, D. Verrier, O. J. Manzoni, and P. Chavis
NMDA Receptor Surface Trafficking and Synaptic Subunit Composition Are Developmentally Regulated by the Extracellular Matrix Protein Reelin
J. Neurosci.,
September 19, 2007;
27(38):
10165 - 10175.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Henneberger, S. J. Redman, and R. Grantyn
Cortical Efferent Control of Subcortical Sensory Neurons by Synaptic Disinhibition
Cereb Cortex,
September 1, 2007;
17(9):
2039 - 2049.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. A. Razak and S. L. Pallas
Inhibitory Plasticity Facilitates Recovery of Stimulus Velocity Tuning in the Superior Colliculus after Chronic NMDA Receptor Blockade
J. Neurosci.,
July 4, 2007;
27(27):
7275 - 7283.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Erazo-Fischer, J. Striessnig, and H. Taschenberger
The Role of Physiological Afferent Nerve Activity during In Vivo Maturation of the Calyx of Held Synapse
J. Neurosci.,
February 14, 2007;
27(7):
1725 - 1737.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Groc, M. Heine, S. L. Cousins, F. A. Stephenson, B. Lounis, L. Cognet, and D. Choquet
NMDA receptor surface mobility depends on NR2A-2B subunits
PNAS,
December 5, 2006;
103(49):
18769 - 18774.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Arsenault and Z.-w. Zhang
Developmental remodelling of the lemniscal synapse in the ventral basal thalamus of the mouse
J. Physiol.,
May 15, 2006;
573(1):
121 - 132.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. W. Barnett, R. F. Watson, T. Vitalis, K. Porter, N. H. Komiyama, P. N. Stoney, T. H. Gillingwater, S. G. N. Grant, and P. C. Kind
Synaptic Ras GTPase Activating Protein Regulates Pattern Formation in the Trigeminal System of Mice
J. Neurosci.,
February 1, 2006;
26(5):
1355 - 1365.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. M. Carrasco, K. A. Razak, and S. L. Pallas
Visual Experience Is Necessary for Maintenance But Not Development of Receptive Fields in Superior Colliculus
J Neurophysiol,
September 1, 2005;
94(3):
1962 - 1970.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Galvan, R. M. Villalba, S. M. West, N. T. Maidment, L. C. Ackerson, Y. Smith, and T. Wichmann
GABAergic Modulation of the Activity of Globus Pallidus Neurons in Primates: In Vivo Analysis of the Functions of GABA Receptors and GABA Transporters
J Neurophysiol,
August 1, 2005;
94(2):
990 - 1000.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Colonnese, J.-P. Zhao, and M. Constantine-Paton
NMDA Receptor Currents Suppress Synapse Formation on Sprouting Axons In Vivo
J. Neurosci.,
February 2, 2005;
25(5):
1291 - 1303.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Townsend, Y. Liu, and M. Constantine-Paton
Retina-Driven Dephosphorylation of the NR2A Subunit Correlates with Faster NMDA Receptor Kinetics at Developing Retinocollicular Synapses
J. Neurosci.,
December 8, 2004;
24(49):
11098 - 11107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. G. Cull-Candy and D. N. Leszkiewicz
Role of Distinct NMDA Receptor Subtypes at Central Synapses
Sci. Signal.,
October 19, 2004;
2004(255):
re16 - re16.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-X. Tao, G. Rumbaugh, G.-D. Wang, R. S. Petralia, C. Zhao, F. W. Kauer, F. Tao, M. Zhuo, R. J. Wenthold, S. N. Raja, et al.
Impaired NMDA Receptor-Mediated Postsynaptic Function and Blunted NMDA Receptor-Dependent Persistent Pain in Mice Lacking Postsynaptic Density-93 Protein
J. Neurosci.,
July 30, 2003;
23(17):
6703 - 6712.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Yoshii, M. H. Sheng, and M. Constantine-Paton
Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons
PNAS,
February 4, 2003;
100(3):
1334 - 1339.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Townsend, A. Yoshii, M. Mishina, and M. Constantine-Paton
Developmental loss of miniature N-methyl-D-aspartate receptor currents in NR2A knockout mice
PNAS,
February 4, 2003;
100(3):
1340 - 1345.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Colonnese, J. Shi, and M. Constantine-Paton
Chronic NMDA Receptor Blockade From Birth Delays the Maturation of NMDA Currents, but Does Not Affect AMPA/Kainate Currents
J Neurophysiol,
January 1, 2003;
89(1):
57 - 68.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Henneberger, R. Juttner, T. Rothe, and R. Grantyn
Postsynaptic Action of BDNF on GABAergic Synaptic Transmission in the Superficial Layers of the Mouse Superior Colliculus
J Neurophysiol,
August 1, 2002;
88(2):
595 - 603.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Shi, S. M. Aamodt, M. Townsend, and M. Constantine-Paton
Developmental Depression of Glutamate Neurotransmission by Chronic Low-Level Activation of NMDA Receptors
J. Neurosci.,
August 15, 2001;
21(16):
6233 - 6244.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Colonnese and M. Constantine-Paton
Chronic NMDA Receptor Blockade from Birth Increases the Sprouting Capacity of Ipsilateral Retinocollicular Axons without Disrupting Their Early Segregation
J. Neurosci.,
March 1, 2001;
21(5):
1557 - 1568.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Taschenberger and H. von Gersdorff
Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity
J. Neurosci.,
December 15, 2000;
20(24):
9162 - 9173.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. D. Hohnke, S. Oray, and M. Sur
Activity-Dependent Patterning of Retinogeniculate Axons Proceeds with a Constant Contribution from AMPA and NMDA Receptors
J. Neurosci.,
November 1, 2000;
20(21):
8051 - 8060.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Ozen, G. J. Augustine, and W. C. Hall
Contribution of Superficial Layer Neurons to Premotor Bursts in the Superior Colliculus
J Neurophysiol,
July 1, 2000;
84(1):
460 - 471.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. M. Aamodt, J. Shi, M. T. Colonnese, W. Veras, and M. Constantine-Paton
Chronic NMDA Exposure Accelerates Development of GABAergic Inhibition in the Superior Colliculus
J Neurophysiol,
March 1, 2000;
83(3):
1580 - 1591.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. White, F. S. Livingston, and R. Mooney
Androgens Modulate NMDA Receptor-Mediated EPSCs in the Zebra Finch Song System
J Neurophysiol,
November 1, 1999;
82(5):
2221 - 2234.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. L. Stark and D. J. Perkel
Two-Stage, Input-Specific Synaptic Maturation in a Nucleus Essential for Vocal Production in the Zebra Finch
J. Neurosci.,
October 15, 1999;
19(20):
9107 - 9116.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F.-S. Lo and R. R. Mize
Retinal Input Induces Three Firing Patterns in Neurons of the Superficial Superior Colliculus of Neonatal Rats
J Neurophysiol,
February 1, 1999;
81(2):
954 - 958.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. D. Hohnke and M. Sur
Stable Properties of Spontaneous EPSCs and Miniature Retinal EPSCs during the Development of ON/OFF Sublamination in the Ferret Lateral Geniculate Nucleus
J. Neurosci.,
January 1, 1999;
19(1):
236 - 247.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. J. King, J. W. H. Schnupp, and I. D. Thompson
Signals from the Superficial Layers of the Superior Colliculus Enable the Development of the Auditory Space Map in the Deeper Layers
J. Neurosci.,
November 15, 1998;
18(22):
9394 - 9408.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Bardoni, P. C. Magherini, and A. B. MacDermott
NMDA EPSCs at Glutamatergic Synapses in the Spinal Cord Dorsal Horn of the Postnatal Rat
J. Neurosci.,
August 15, 1998;
18(16):
6558 - 6567.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Strack and R. J. Colbran
Autophosphorylation-dependent Targeting of Calcium/ Calmodulin-dependent Protein Kinase II by the NR2B Subunit of the N-Methyl- D-aspartate Receptor
J. Biol. Chem.,
August 14, 1998;
273(33):
20689 - 20692.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F.-S. Lo and R. R. Mize
Synaptic Regulation of L-Type Ca2+ Channel Activity and Long-Term Depression during Refinement of the Retinocollicular Pathway in Developing Rodent Superior Colliculus
J. Neurosci.,
February 1, 2000;
20(3):
RC58 - RC58.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|