A model of stimulus-specific neural assemblies in the insect antennal lobe.
It has been proposed that synchronized neural assemblies in the antennal lobe of insects encode the identity of olfactory stimuli. In response to an odor, some projection neurons exhibit synchronous firing, phase-locked to the oscillations of the field potential, whereas others do not. Experimental data indicate that neural synchronization and field oscillations are induced by fast GABA(A)-type inhibition, but it remains unclear how desynchronization occurs. We hypothesize that slow inhibition plays a key role in desynchronizing projection neurons. Because synaptic noise is believed to be the dominant factor that limits neuronal reliability, we consider a computational model of the antennal lobe in which a population of oscillatory neurons interact through unreliable GABA(A) and GABA(B) inhibitory synapses. From theoretical analysis and extensive computer simulations, we show that transmission failures at slow GABA(B) synapses make the neural response unpredictable. Depending on the balance between GABA(A) and GABA(B) inputs, particular neurons may either synchronize or desynchronize. These findings suggest a wiring scheme that triggers stimulus-specific synchronized assemblies. Inhibitory connections are set by Hebbian learning and selectively activated by stimulus patterns to form a spiking associative memory whose storage capacity is comparable to that of classical binary-coded models. We conclude that fast inhibition acts in concert with slow inhibition to reformat the glomerular input into odor-specific synchronized neural assemblies.
Martinez
Dominique
D
LORIA, Campus Scientifique, Vandoeuvre-lès-Nancy, France. dominique.martinez@loria.fr
Montejo
Noelia
N
D000818:Animals; D001244:Association; D005246:Feedback / Q000502:physiology; D007313:Insecta / Q000502:physiology*; D007700:Kinetics; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D009433:Neural Inhibition; D009833:Olfactory Pathways / Q000502:physiology*; D018034:Olfactory Receptor Neurons / Q000502:physiology; D046709:Pattern Recognition, Physiological; D012903:Smell / Q000502:physiology; D009435:Synaptic Transmission / Q000502:physiology; D049490:Systems Biology; D013997:Time Factors; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D005680:gamma-Aminobutyric Acid
J Neurosci. 1996 Oct 15;16(20):6402-13
8815919
Nat Neurosci. 2001 Mar;4(3):297-303
11224547
Science. 1994 Sep 23;265(5180):1872-5
17797226
Trends Neurosci. 1996 Nov;19(11):489-96
8931275
Biol Bull. 2000 Oct;199(2):170-1
11081718
Science. 1996 Nov 8;274(5289):976-9
8875938
Eur J Neurosci. 2003 Oct;18(8):2119-32
14622173
Nature. 2007 Nov 29;450(7170):623-5
18046390
Front Zool. 2006 Dec 29;3:22
17196109
J Comput Neurosci. 2003 Jul-Aug;15(1):91-103
12843697
Neural Comput. 2005 Dec;17(12):2548-70
16212762
Nat Rev Neurosci. 2002 Nov;3(11):884-95
12415296
J Comp Physiol A. 1998 Jun;182(6):703-14
9631552
Science. 2004 Jan 16;303(5656):366-70
14684826
PLoS Comput Biol. 2006 Aug 18;2(8):e103
16933980
Nat Neurosci. 2004 Aug;7(8):862-71
15273692
J Neurophysiol. 2002 Feb;87(2):1106-17
11826074
Neuron. 2002 Oct 24;36(3):463-74
12408848
J Comput Neurosci. 1994 Dec;1(4):313-21
8792237
Neural Comput. 2006 Jan;18(1):10-25
16354378
Nature. 1997 Nov 6;390(6655):70-4
9363891
Neuron. 2005 May 5;46(3):483-92
15882647
J Physiol. 2002 Jul 15;542(Pt 2):355-67
12122137
J Neurosci. 2005 Apr 6;25(14):3521-30
15814782
Science. 2004 Jun 25;304(5679):1926-9
15218136
J Neurosci. 1998 Sep 1;18(17):6790-802
9712650
Neuron. 2007 Dec 6;56(5):838-50
18054860
J Comput Neurosci. 1998 Mar;5(1):5-16
9580271
J Neurosci. 2005 Oct 5;25(40):9069-79
16207866
Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11826-31
17596338
Neural Comput. 2006 May;18(5):1066-110
16595058
Behav Neurosci. 2000 Jun;114(3):514-25
10883802
Cell. 2007 Feb 9;128(3):601-12
17289577
Nat Neurosci. 2002 Jun;5(6):557-65
12006983
J Comput Neurosci. 1998 Dec;5(4):407-20
9877022
Nature. 1969 Jun 7;222(5197):960-2
5789326
Neuron. 2001 May;30(2):553-67
11395014
Neural Comput. 2003 Mar;15(3):509-38
12620157
Nat Neurosci. 2005 Oct;8(10):1283-4
16189532
Neuron. 2007 Apr 5;54(1):89-103
17408580
PLoS Biol. 2006 Jun;4(6):e163
16689623
Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10380-3
7937958
Cell. 2002 Apr 19;109(2):243-55
12007410
J Neurophysiol. 2006 Apr;95(4):2678-91
16381804
Annu Rev Entomol. 2000;45:203-31
10761576
J Neurophysiol. 2005 Jun;93(6):3410-7
15673548
J Neurophysiol. 2008 Jan;99(1):277-83
17928562
J Neurosci. 2006 Sep 6;26(36):9332-9
16957089
Neuron. 2001 May;30(2):569-81
11395015
J Neurosci. 2006 Apr 5;26(14):3646-55
16597718
Neural Comput. 1996 Jul 1;8(5):979-1001
8697231
Cell. 2002 Apr 19;109(2):229-41
12007409
J Neurophysiol. 2007 Dec;98(6):3134-42
17855585