Altered sensory experience induces targeted rewiring of local excitatory connections in mature neocortex.
Experience-dependent plasticity in adulthood is slower than during development. Previous experience can accelerate adult cortical plasticity. However, the contributions of functional synaptic changes and modifications in neuronal structure to the acceleration of adult cortical plasticity remain unclear. If structural remodeling was important then it should be exhibited by neuronal connections that have altered during plasticity. We trimmed rodents' whiskers to induce experience-dependent plasticity and reconstructed pairs of layer 2/3 (L2/3) pyramidal neurons after electrophysiological recording. We reported recently that local excitatory connections strengthen without a change in synapse number in cortex with retained sensory input (spared) (Cheetham et al., 2007). Here, we show that strengthened connections are rewired. The rewiring involves remodeling of the axonal arbor of excitatory connections with only minor changes in postsynaptic dendritic trees. The axonal remodeling resulted in a greater length of presynaptic axon close to postsynaptic dendrites at existing local excitatory connections in spared cortex. In control cortex, the length of axon close to dendrite in unconnected pairs of L2/3 pyramidal neurons was similar to that in synaptically connected pairs of L2/3 pyramidal neurons. This finding suggests that the probability of forming a synapse and, therefore, establishing a connection, is not driven solely by the length of axon close to dendrite. The axonal remodeling that we describe is not associated with altered synapse number, but instead increases the number of sites where synapses could be formed between synaptically connected neurons with minimal structural changes. This enables rapid and cost-efficient rewiring of local excitatory connections when re-exposed to similarly altered sensory experience in adulthood.
Cheetham
Claire E J
CE
Medical Research Centre for Neurodegeneration Research, King's College London, London SE5 8AF, United Kingdom.
Hammond
Martin S L
MS
McFarlane
Rachael
R
Finnerty
Gerald T
GT
D000704:Analysis of Variance; D000818:Animals; D000831:Animals, Newborn; D001931:Brain Mapping; D003712:Dendrites / Q000502:physiology / Q000648:ultrastructure; D049229:Dendritic Spines / Q000502:physiology / Q000648:ultrastructure; D066298:In Vitro Techniques; D018613:Microscopy, Confocal; D015233:Models, Statistical; D019579:Neocortex / Q000166:cytology* / Q000254:growth & development / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology; D009473:Neuronal Plasticity; D017966:Pyramidal Cells / Q000166:cytology / Q000502:physiology*; D051381:Rats; D012683:Sensory Deprivation / Q000502:physiology; D013569:Synapses / Q000502:physiology*; D014738:Vibrissae / Q000294:innervation*
J Neurocytol. 2002 Mar-Jun;31(3-5):337-46
12815251
J Neurosci. 2001 May 1;21(9):3161-74
11312301
Somatosens Mot Res. 1999;16(2):122-38
10449061
Nature. 2004 Oct 14;431(7010):775-81
15483598
Annu Rev Psychol. 1987;38:129-51
3548573
Exp Neurol. 2003 Dec;184(2):737-45
14769365
Nature. 2006 Jun 22;441(7096):979-83
16791195
Biometrics. 1986 Mar;42(1):121-30
3719049
Curr Opin Neurobiol. 2003 Jun;13(3):372-83
12850223
J Neurosci. 1998 Oct 15;18(20):8300-10
9763474
PLoS Biol. 2005 Aug;3(8):e272
16026180
Biol Cybern. 2003 Mar;88(3):210-8
12647228
Neuron. 2005 Apr 21;46(2):181-9
15848798
J Comp Neurol. 1991 Apr 8;306(2):332-43
1711059
Curr Opin Neurobiol. 2007 Aug;17(4):456-64
17714932
Nature. 2005 Mar 10;434(7030):221-5
15759002
J Neurosci. 2007 Mar 28;27(13):3456-65
17392462
J Cell Sci. 1969 Sep;5(2):509-29
5362339
Behav Brain Res. 1989 Jan 1;31(3):285-9
2914080
Annu Rev Neurosci. 1998;21:149-86
9530495
Nat Neurosci. 2006 Sep;9(9):1117-24
16892056
Neuroscience. 1979;4(9):1275-97
492537
J Comp Neurol. 1990 Jan 1;291(1):43-54
2298929
Neuron. 2006 Mar 16;49(6):877-87
16543135
Stat Methods Med Res. 1995 Sep;4(3):187-96
8548102
Neuron. 2001 Mar;29(3):779-96
11301036
Cereb Cortex. 2004 Jun;14(6):655-64
15054062
PLoS Biol. 2006 Feb;4(2):e29
16366735
J Neurophysiol. 1992 May;67(5):1031-56
1597696
J Neurocytol. 1976 Feb;5(1):63-84
1249593
J Neurosci. 1999 Oct 15;19(20):9117-25
10516329
Science. 1992 Jan 10;255(5041):209-12
1372754
J Neurosci. 2006 Aug 16;26(33):8451-64
16914670
Neuroscience. 2002;111(4):799-814
12031405
Biol Cybern. 2000 Feb;82(2):111-21
10664098
Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7587-91
10377459
Annu Rev Neurosci. 2005;28:127-56
16022592
Science. 1998 Nov 6;282(5391):1117-21
9804549
Nat Neurosci. 2006 Jan;9(1):127-32
16327785
Neuron. 2001 Sep 13;31(5):681-97
11567610
Neuron. 2006 Nov 22;52(4):577-85
17114043
J Comp Neurol. 2004 Nov 1;479(1):56-69
15389615
Cereb Cortex. 2000 Jan;10(1):23-31
10639392
Nat Neurosci. 2005 Feb;8(2):140-2
15657598
Nat Neurosci. 2005 Jan;8(1):93-8
15608636
Neuron. 2002 Apr 11;34(2):275-88
11970869
Nature. 1994 Apr 21;368(6473):737-40
8152484
J Neurosci. 2006 Dec 6;26(49):12717-26
17151275
Neuron. 2001 May;30(2):315-8
11394995
Science. 1998 Mar 6;279(5356):1531-3
9488651
Nature. 2004 Oct 14;431(7010):782-8
15483599
Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4631-6
15767584
Proc Natl Acad Sci U S A. 2005 Jan 18;102(3):880-5
15630093
Nat Neurosci. 2005 Jun;8(6):782-90
15880111
J Neurophysiol. 1996 Apr;75(4):1714-29
8727408
J Neurosci. 1999 Jun 1;19(11):4388-406
10341241
Exp Neurol. 1978 Dec;62(3):658-77
750216
Neuron. 2006 Mar 16;49(6):861-75
16543134
Neuron. 1999 Nov;24(3):623-37
10595514
Nat Neurosci. 2007 May;10(5):549-51
17417634
Nature. 2002 Dec 19-26;420(6917):788-94
12490942
Science. 1994 Sep 23;265(5180):1885-8
8091215
Exp Brain Res. 1998 Nov;123(1-2):110-6
9835399
Exp Neurol. 1987 May;96(2):262-78
3569455
Nature. 2005 Jul 14;436(7048):261-5
16015331
Psychol Bull. 1953 Nov;50(6):401-31
13112332
Nat Neurosci. 2003 Nov;6(11):1201-7
14528309
J Neurosci. 2006 Mar 29;26(13):3604-14
16571769
Neuron. 2005 Jan 20;45(2):279-91
15664179
J Neurosci. 2004 Sep 29;24(39):8441-53
15456817
J Neurosci. 2006 Mar 15;26(11):3021-9
16540580
Neuron. 2001 Aug 2;31(2):305-15
11502260