Synaptic Plasticity in Rat Hippocampal Slice Cultures: Local "Hebbian" Conjunction of Pre- and Postsynaptic Stimulation Leads to Distributed Synaptic Enhancement
A central theme in neurobiology is
the search for the mechanisms underlying learning and memory. Since the
seminal work, first of Cajal and later of Hebb, the synapse is thought
to be the basic "storing unit." Hebb proposed that information is
stored by correlation: synapses between neurons, which are often
coactive, are enhanced. Several recent findings suggest that such a
mechanism is indeed operative in the central nervous system. Pairing of
activity on presynaptic fibers with strong postsynaptic depolarization
results in synaptic enhancement. While there is substantial evidence in
favor of a postsynaptic locus for detection of the synchronous pre- and
postsynaptic event and subsequent initiation of synaptic enhancement,
the locus of this enhancement and its ensuing persistence is still
disputed: both pre- and postsynaptic contributions have been suggested.
In all previous studies, the enhancement was presumed to be specific to
the synapses where synchronous pre- and postsynaptic stimulation was
applied. We report here that two recording techniques--optical
recording, using voltage-sensitive dyes, and double intracellular
recordings--reveal that synaptic enhancement is not restricted to the
stimulated cell. Although we paired single afferent volleys with
intracellular stimulation confined to one postsynaptic cell, we found
that strengthening also occurred on synapses between the stimulated
presynaptic fibers and neighboring cells. This suggests that synaptic
enhancement by the "paired-stimulation paradigm" is not local on the
presynaptic axons and that, in fact, the synapses of many neighboring
postsynaptic cells are enhanced.
This article has been cited by other articles in HighWire Press-hosted journals:
|
A. M. Apergis-Schoute, J. Debiec, V. Doyere, J. E. LeDoux, and G. E. Schafe Auditory Fear Conditioning and Long-Term Potentiation in the Lateral Amygdala Require ERK/MAP Kinase Signaling in the Auditory Thalamus: A Role for Presynaptic Plasticity in the Fear System J. Neurosci., June 15, 2005; 25(24): 5730 - 5739. [Abstract] [Full Text] [PDF] |
||||
|
K. Nakayama, K. Kiyosue, and T. Taguchi Diminished Neuronal Activity Increases Neuron-Neuron Connectivity Underlying Silent Synapse Formation and the Rapid Conversion of Silent to Functional Synapses J. Neurosci., April 20, 2005; 25(16): 4040 - 4051. [Abstract] [Full Text] [PDF] |
||||
|
A. Burette, U. Zabel, R. J. Weinberg, H. H. H. W. Schmidt, and J. G. Valtschanoff Synaptic Localization of Nitric Oxide Synthase and Soluble Guanylyl Cyclase in the Hippocampus J. Neurosci., October 15, 2002; 22(20): 8961 - 8970. [Abstract] [Full Text] [PDF] |
||||
|
H. W. Tao and M.-m. Poo Retrograde signaling at central synapses PNAS, September 25, 2001; 98(20): 11009 - 11015. [Abstract] [Full Text] [PDF] |
||||
|
R. Kempter, C. Leibold, H. Wagner, and J. L. van Hemmen Formation of temporal-feature maps by axonal propagation of synaptic learning PNAS, March 27, 2001; 98(7): 4166 - 4171. [Abstract] [Full Text] [PDF] |
||||
|
J. H. Schaffhausen, T. M. Fischer, and T. J. Carew Contirbution of Postsynaptic Ca2+ to the Induction of Posttetanic Potentiation in the Neural Circuit for Siphon Withdrawal in Aplysia J. Neurosci., March 1, 2001; 21(5): 1739 - 1749. [Abstract] [Full Text] |
||||
|
G. J. Mitchison and N. V. Swindale Can Hebbian Volume Learning Explain Discontinuities in Cortical Maps? Neural Comput., October 1, 1999; 11(7): 1519 - 1526. [Abstract] [Full Text] |
||||
|
H.-z. W. Tao, L. I. Zhang, G.-q. Bi, and M.-m. Poo Selective Presynaptic Propagation of Long-Term Potentiation in Defined Neural Networks J. Neurosci., May 1, 2000; 20(9): 3233 - 3243. [Abstract] [Full Text] |
||||
|
K. Stefan, E. Kunesch, L. G. Cohen, R. Benecke, and J. Classen Induction of plasticity in the human motor cortex by paired associative stimulation Brain, March 1, 2000; 123(3): 572 - 584. [Abstract] [Full Text] |
||||
|
H. Dodt, M. Eder, A. Frick, and W. Zieglgänsberger Precisely Localized LTD in the Neocortex Revealed by Infrared-Guided Laser Stimulation Science, October 1, 1999; 286(5437): 110 - 113. [Abstract] [Full Text] |
||||
|
Y.-F. Lu, E. R. Kandel, and R. D. Hawkins Nitric Oxide Signaling Contributes to Late-Phase LTP and CREB Phosphorylation in the Hippocampus J. Neurosci., December 1, 1999; 19(23): 10250 - 10261. [Abstract] [Full Text] |
||||
|
T. M. Jay, E. Zilkha, and T. P. Obrenovitch Long-Term Potentiation in the Dentate Gyrus Is Not Linked to Increased Extracellular Glutamate Concentration J Neurophysiol, April 1, 1999; 81(4): 1741 - 1748. [Abstract] [Full Text] |
||||
|
S. Chang and S. V. Popov Long-range signaling within growing neurites mediated by neurotrophin-3 PNAS, March 30, 1999; 96(7): 4095 - 4100. [Abstract] [Full Text] [PDF] |
||||
|
R. M. FITZSIMONDS and M.-M. POO Retrograde Signaling in the Development and Modification of Synapses Physiol Rev, January 1, 1998; 78(1): 143 - 170. [Abstract] [Full Text] |
||||
|
X.-h. Wang, B. Berninger, and M.-m. Poo Localized Synaptic Actions of Neurotrophin-4 J. Neurosci., July 1, 1998; 18(13): 4985 - 4992. [Abstract] [Full Text] |
||||
|
Y. Goda and C. F. Stevens Readily releasable pool size changes associated with long term depression PNAS, February 3, 1998; 95(3): 1283 - 1288. [Abstract] [Full Text] [PDF] |
||||