 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, August 1, 2001, 21(15):5568-5573
Associative Learning Elicits the Formation of Multiple-Synapse Boutons
Yuri Geinisman1, Robert W. Berry1, John F. Disterhoft1, John M. Power2, and Eddy A. Van der Zee3 1 Department of Cell and Molecular Biology, Northwestern University Medical School, Chicago, Illinois 60611, 2 Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra ACT 2601, Australia, and 3 Department of Zoology, University of Groningen, 9751 NN Haren, The Netherlands
The formation of new synapses has been suggested to underlie learning and memory. However, previous work from this laboratory has demonstrated that hippocampus-dependent associative learning does not induce a net gain in the total number of hippocampal synapses and, hence, a net synaptogenesis. The aim of the present work was to determine whether associative learning involves a specific synaptogenesis confined to the formation of multiple-synapse boutons (MSBs) that synapse with more than one dendritic spine. We used the behavioral paradigm of trace eyeblink conditioning, which is a hippocampus-dependent form of associative learning. Conditioned rabbits were given daily 80-trial sessions to a criterion of 80% conditioned responses in a session. During each trial, the conditioned stimulus (tone) and the unconditioned stimulus (corneal airpuff) were presented with an intervening trace interval of 500 msec. Brain tissue was taken for morphological analyses 24 hr after the last session. Unbiased stereological methods were used for obtaining estimates of the total number of MSBs in the stratum radiatum of hippocampal subfield CA1. The results showed that the total number of MSBs was significantly increased in conditioned rabbits as compared with pseudoconditioned or unstimulated controls. This conditioning-induced change, which occurs without a net synaptogenesis, reflects a specific synaptogenesis resulting in MSB formation. Models of the latter process are proposed. The models postulate that it requires spine motility and may involve the relocation of existing spines from nonactivated boutons or the outgrowth of newly formed spines for specific synaptogenesis with single-synapse boutons activated by the conditioning stimulation.
Key words: associative learning; trace eyeblink conditioning; hippocampus; CA1 stratum radiatum; multiple-synapse boutons; synaptic plasticity; synaptogenesis; spine motility
Copyright © 2001 Society for Neuroscience 0270-6474/01/21155568-06$05.00/0
This article has been cited by other articles:
J. Waddell, D. A. Bangasser, and T. J. Shors
The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females
J. Neurosci., May 14, 2008; 28(20): 5290 - 5294.
[Abstract] [Full Text] [PDF]
J. Hongpaisan and D. L. Alkon
A structural basis for enhancement of long-term associative memory in single dendritic spines regulated by PKC
PNAS, December 4, 2007; 104(49): 19571 - 19576.
[Abstract] [Full Text] [PDF]
V. Nagy, O. Bozdagi, and G. W. Huntley
The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory
Learn. Mem., September 25, 2007; 14(10): 655 - 664.
[Abstract] [Full Text] [PDF]
M. Mokin, Z. Zheng, and J. Keifer
Conversion of Silent Synapses Into the Active Pool by Selective GluR1-3 and GluR4 AMPAR Trafficking During In Vitro Classical Conditioning
J Neurophysiol, September 1, 2007; 98(3): 1278 - 1286.
[Abstract] [Full Text] [PDF]
M. H. Milekic, G. Pollonini, and C. M. Alberini
Temporal requirement of C/EBP{beta} in the amygdala following reactivation but not acquisition of inhibitory avoidance
Learn. Mem., July 18, 2007; 14(7): 504 - 511.
[Abstract] [Full Text] [PDF]
A. C.W. Weeks, S. Connor, R. Hinchcliff, J. C. LeBoutillier, R. F. Thompson, and T. L. Petit
Eye-blink conditioning is associated with changes in synaptic ultrastructure in the rabbit interpositus nuclei
Learn. Mem., June 5, 2007; 14(6): 385 - 389.
[Abstract] [Full Text] [PDF]
A. Garcia-Osta, P. Tsokas, G. Pollonini, E. M. Landau, R. Blitzer, and C. M. Alberini
MuSK expressed in the brain mediates cholinergic responses, synaptic plasticity, and memory formation.
J. Neurosci., July 26, 2006; 26(30): 7919 - 7932.
[Abstract] [Full Text] [PDF]
C. Hanus, M.-V. Ehrensperger, and A. Triller
Activity-dependent movements of postsynaptic scaffolds at inhibitory synapses.
J. Neurosci., April 26, 2006; 26(17): 4586 - 4595.
[Abstract] [Full Text] [PDF]
T. Hajszan and N. J. MacLusky
Neurologic links between epilepsy and depression in women: Is hippocampal neuroplasticity the key?
Neurology, March 28, 2006; 66(66_suppl_3): S13 - S22.
[Abstract] [Full Text]
L. Shi, M. C. Linville, E. W. Tucker, W. E. Sonntag, and J. K. Brunso-Bechtold
Differential Effects of Aging and Insulin-like Growth Factor-1 on Synapses in CA1 of Rat Hippocampus
Cereb Cortex, May 1, 2005; 15(5): 571 - 577.
[Abstract] [Full Text] [PDF]
D. A. Richards, J. M. Mateos, S. Hugel, V. de Paola, P. Caroni, B. H. Gahwiler, and R. A. McKinney
Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures
PNAS, April 26, 2005; 102(17): 6166 - 6171.
[Abstract] [Full Text] [PDF]
N. Gruest, P. Richer, and B. Hars
Memory Consolidation and Reconsolidation in the Rat Pup Require Protein Synthesis
J. Neurosci., November 17, 2004; 24(46): 10488 - 10492.
[Abstract] [Full Text] [PDF]
O. Stork, A. Zhdanov, A. Kudersky, T. Yoshikawa, K. Obata, and H.-C. Pape
Neuronal Functions of the Novel Serine/Threonine Kinase Ndr2
J. Biol. Chem., October 29, 2004; 279(44): 45773 - 45781.
[Abstract] [Full Text] [PDF]
W. W. Wu, C. S. Chan, and J. F. Disterhoft
Slow Afterhyperpolarization Governs the Development of NMDA Receptor-Dependent Afterdepolarization in CA1 Pyramidal Neurons During Synaptic Stimulation
J Neurophysiol, October 1, 2004; 92(4): 2346 - 2356.
[Abstract] [Full Text] [PDF]
J. Spacek and K. M. Harris
Trans-Endocytosis via Spinules in Adult Rat Hippocampus
J. Neurosci., April 28, 2004; 24(17): 4233 - 4241.
[Abstract] [Full Text] [PDF]
K. M. Christian and R. F. Thompson
Neural Substrates of Eyeblink Conditioning: Acquisition and Retention
Learn. Mem., November 1, 2003; 10(6): 427 - 455.
[Abstract] [Full Text] [PDF]
J. A. Harvey
Role of the Serotonin 5-HT2A Receptor in Learning
Learn. Mem., September 1, 2003; 10(5): 355 - 362.
[Abstract] [Full Text] [PDF]
K. Matsumoto-Miyai, A. Ninomiya, H. Yamasaki, H. Tamura, Y. Nakamura, and S. Shiosaka
NMDA-Dependent Proteolysis of Presynaptic Adhesion Molecule L1 in the Hippocampus by Neuropsin
J. Neurosci., August 27, 2003; 23(21): 7727 - 7736.
[Abstract] [Full Text] [PDF]
S. A. Aicher, S. Sharma, and J. L. Mitchell
Structural Changes in AMPA-Receptive Neurons in the Nucleus of the Solitary Tract of Spontaneously Hypertensive Rats
Hypertension, June 1, 2003; 41(6): 1246 - 1252.
[Abstract] [Full Text] [PDF]
B. Leuner, J. Falduto, and T. J. Shors
Associative Memory Formation Increases the Observation of Dendritic Spines in the Hippocampus
J. Neurosci., January 15, 2003; 23(2): 659 - 665.
[Abstract] [Full Text] [PDF]
G. M. G. Shepherd, M. Raastad, and P. Andersen
General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum
PNAS, April 30, 2002; 99(9): 6340 - 6345.
[Abstract] [Full Text] [PDF]
P. Jourdain, I. Nikonenko, S. Alberi, and D. Muller
Remodeling of Hippocampal Synaptic Networks by a Brief Anoxia-Hypoglycemia
J. Neurosci., April 15, 2002; 22(8): 3108 - 3116.
[Abstract] [Full Text] [PDF]
G. M. G. Shepherd, M. Raastad, and P. Andersen
General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum
PNAS, April 30, 2002; 99(9): 6340 - 6345.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|