Highly nonrandom features of synaptic connectivity in local cortical circuits.
How different is local cortical circuitry from a random network? To answer this question, we probed synaptic connections with several hundred simultaneous quadruple whole-cell recordings from layer 5 pyramidal neurons in the rat visual cortex. Analysis of this dataset revealed several nonrandom features in synaptic connectivity. We confirmed previous reports that bidirectional connections are more common than expected in a random network. We found that several highly clustered three-neuron connectivity patterns are overrepresented, suggesting that connections tend to cluster together. We also analyzed synaptic connection strength as defined by the peak excitatory postsynaptic potential amplitude. We found that the distribution of synaptic connection strength differs significantly from the Poisson distribution and can be fitted by a lognormal distribution. Such a distribution has a heavier tail and implies that synaptic weight is concentrated among few synaptic connections. In addition, the strengths of synaptic connections sharing pre- or postsynaptic neurons are correlated, implying that strong connections are even more clustered than the weak ones. Therefore, the local cortical network structure can be viewed as a skeleton of stronger connections in a sea of weaker ones. Such a skeleton is likely to play an important role in network dynamics and should be investigated further.
Song
Sen
S
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
Sjöström
Per Jesper
PJ
Reigl
Markus
M
Nelson
Sacha
S
Chklovskii
Dmitri B
DB
D000818:Animals; D002450:Cell Communication / Q000502:physiology; D066298:In Vitro Techniques; D009434:Neural Pathways / Q000502:physiology; D009473:Neuronal Plasticity; D009474:Neurons / Q000502:physiology*; D051381:Rats; D015398:Signal Transduction; D013569:Synapses / Q000502:physiology*; D014793:Visual Cortex / Q000502:physiology*
Nature. 1996 Aug 29;382(6594):807-10
8752273
J Physiol. 2003 Aug 15;551(Pt 1):139-53
12813147
Neuron. 2001 Dec 6;32(5):883-98
11738033
Phys Rev Lett. 2003 Oct 17;91(16):168701
14611445
J Comp Neurol. 1985 Aug 15;238(3):263-74
4044915
Science. 2002 Oct 25;298(5594):824-7
12399590
Science. 2003 Dec 12;302(5652):1981-4
14671309
Int Rev Physiol. 1978;17:149-91
359497
Science. 1999 Oct 15;286(5439):509-12
10521342
J Comp Neurol. 1994 Jan 22;339(4):475-94
8144742
Nat Rev Genet. 2004 Feb;5(2):101-13
14735121
Science. 2002 Aug 30;297(5586):1551-5
12202830
Cereb Cortex. 2002 Sep;12(9):936-53
12183393
Nat Neurosci. 1998 Sep;1(5):395-403
10196530
J Physiol. 1999 Nov 15;521 Pt 1:169-90
10562343
BMC Biol. 2004;2:25
15574204
Biol Cybern. 2002 Dec;87(5-6):446-58
12461634
PLoS Biol. 2004 Nov;2(11):e329
15514700
Science. 2002 May 3;296(5569):910-3
11988575
IEEE Trans Biomed Eng. 1989 Jan;36(1):4-14
2646211
Philos Trans R Soc Lond B Biol Sci. 1986 Nov 12;314(1165):1-340
22462104
Nat Neurosci. 1999 Dec;2(12):1098-105
10570487
J Neurophysiol. 1993 Dec;70(6):2354-69
8120587
J Neurosci. 2004 Mar 24;24(12):2989-3001
15044538
Neuron. 2004 Sep 2;43(5):745-57
15339654
Nature. 2003 May 15;423(6937):283-8
12748641
Cereb Cortex. 1997 Sep;7(6):523-33
9276177
Nature. 1995 Nov 16;378(6554):281-4
7477347
J Neurophysiol. 2004 Jul;92(1):600-8
15056678
Neuron. 2003 Feb 6;37(3):499-511
12575956
Neuron. 2003 Aug 14;39(4):641-54
12925278
Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3619-24
10737806
J Neurosci. 1996 May 15;16(10):3209-18
8627359
J Neurosci. 1993 May;13(5):2199-216
8386756
J Neurophysiol. 1995 Mar;73(3):1145-56
7608761
J Bacteriol. 2002 Jan;184(1):152-64
11741855
Science. 1997 Jan 10;275(5297):213-5
8985014
Cereb Cortex. 2003 Jan;13(1):5-14
12466210
Neuron. 2001 Dec 20;32(6):1149-64
11754844
Nature. 1996 Oct 31;383(6603):815-9
8893005
Nat Neurosci. 2000 Jul;3(7):701-7
10862703
J Physiol. 1962 Jan;160:106-54
14449617
Nature. 2001 Mar 8;410(6825):268-76
11258382
Science. 2004 Apr 23;304(5670):559-64
15105494
J Physiol. 1991;440:735-69
1666655
Neural Netw. 2001 Jul-Sep;14(6-7):815-24
11665773
J Neurosci. 2002 Nov 15;22(22):9885-94
12427845
Neuron. 2001 Mar;29(3):691-701
11301028
Phys Rev Lett. 2002 Mar 11;88(10):108701
11909388
J Neurophysiol. 1988 Sep;60(3):909-24
3171666
Science. 2001 Aug 3;293(5531):868-72
11486089
Neuron. 2001 Oct 25;32(2):339-50
11684002
Nature. 1998 Jun 4;393(6684):440-2
9623998
Science. 2004 Mar 5;303(5663):1538-42
15001784
Biol Cybern. 2003 Mar;88(3):210-8
12647228
Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7121-6
9618549
J Physiol. 1997 Apr 15;500 ( Pt 2):409-40
9147328
Nature. 2004 Feb 26;427(6977):839-43
14985762
Neuron. 1992 Dec;9(6):1089-97
1334418
J Neurosci. 1998 Dec 15;18(24):10464-72
9852584
Acta Morphol Hung. 1990;38(3-4):159-67
2102598
J Neurosci. 1999 May 15;19(10):3827-35
10234015
J Neurosci. 2002 Nov 15;22(22):9668-78
12427822