Spike-timing theory of working memory.
Working memory (WM) is the part of the brain's memory system that provides temporary storage and manipulation of information necessary for cognition. Although WM has limited capacity at any given time, it has vast memory content in the sense that it acts on the brain's nearly infinite repertoire of lifetime long-term memories. Using simulations, we show that large memory content and WM functionality emerge spontaneously if we take the spike-timing nature of neuronal processing into account. Here, memories are represented by extensively overlapping groups of neurons that exhibit stereotypical time-locked spatiotemporal spike-timing patterns, called polychronous patterns; and synapses forming such polychronous neuronal groups (PNGs) are subject to associative synaptic plasticity in the form of both long-term and short-term spike-timing dependent plasticity. While long-term potentiation is essential in PNG formation, we show how short-term plasticity can temporarily strengthen the synapses of selected PNGs and lead to an increase in the spontaneous reactivation rate of these PNGs. This increased reactivation rate, consistent with in vivo recordings during WM tasks, results in high interspike interval variability and irregular, yet systematically changing, elevated firing rate profiles within the neurons of the selected PNGs. Additionally, our theory explains the relationship between such slowly changing firing rates and precisely timed spikes, and it reveals a novel relationship between WM and the perception of time on the order of seconds.
Szatmáry
Botond
B
The Neurosciences Institute, San Diego, California, United States of America.
Izhikevich
Eugene M
EM
D000818:Animals; D001921:Brain / Q000502:physiology; D003198:Computer Simulation; D057567:Memory, Long-Term / Q000502:physiology; D008570:Memory, Short-Term / Q000502:physiology*; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000502:physiology; D013569:Synapses / Q000502:physiology; D009435:Synaptic Transmission / Q000502:physiology; D013998:Time Perception / Q000502:physiology
Neuron. 2007 Feb 1;53(3):427-38
17270738
Science. 2008 Sep 5;321(5894):1322-7
18772431
Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13481-6
8942960
Psychol Rev. 1956 Mar;63(2):81-97
13310704
Neural Comput. 2005 Mar;17(3):691-713
15802011
J Neurosci. 1999 Nov 1;19(21):9587-603
10531461
Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5175-80
17360369
Neural Comput. 2006 Feb;18(2):245-82
16378515
Behav Brain Res. 1998 Mar;91(1-2):1-13
9578434
IEEE Trans Neural Netw. 2003;14(6):1569-72
18244602
J Neurophysiol. 2000 May;83(5):3031-41
10805698
Nat Neurosci. 2004 Feb;7(2):170-7
14730306
Neuron. 2009 May 14;62(3):413-25
19447096
Cereb Cortex. 2003 Nov;13(11):1196-207
14576211
PLoS Comput Biol. 2007 Sep;3(9):1679-700
17845070
Neuron. 2009 Feb 26;61(4):621-34
19249281
Neuron. 2005 Feb 3;45(3):419-31
15694328
J Neurosci. 1993 Aug;13(8):3406-20
8340815
Trends Neurosci. 2001 Aug;24(8):455-63
11476885
J Neurophysiol. 1992 Aug;68(2):605-19
1527578
Cereb Cortex. 2004 Aug;14(8):933-44
15142958
Science. 2008 Mar 14;319(5869):1543-6
18339943
Prog Neurobiol. 2004 Sep;74(1):1-58
15381316
Science. 1971 Aug 13;173(3997):652-4
4998337
Nature. 2007 Aug 9;448(7154):709-13
17581587
J Neurophysiol. 2003 Nov;90(5):3441-54
12773500
J Neurophysiol. 1989 Feb;61(2):331-49
2918358
Nature. 2000 Mar 16;404(6775):285-9
10749211
Front Neurosci. 2008 Jul 14;2(1):114-22
18982114
J Neurophysiol. 1985 Nov;54(5):1346-62
4078619
Nat Neurosci. 1998 Aug;1(4):273-5
10195158
Science. 1997 Jan 10;275(5297):213-5
8985014
J Neurosci. 2006 Jun 21;26(25):6704-15
16793878
J Neurophysiol. 1994 Feb;71(2):437-53
8176419
Psychon Bull Rev. 2001 Sep;8(3):568-78
11700909
Science. 2008 Feb 22;319(5866):1108-11
18292344
J Neurophysiol. 2005 Oct;94(4):2275-83
16160088
J Cogn Neurosci. 2010 Nov;22(11):2530-40
19925206
Nat Neurosci. 2007 Jan;10(1):100-7
17173043
Nat Rev Neurosci. 2005 May;6(5):399-407
15861182
PLoS Comput Biol. 2008 May 16;4(5):e1000073
18464917
Nat Neurosci. 2000 Sep;3(9):919-26
10966623
Nat Neurosci. 2008 Jul;11(7):823-33
18516033
Nat Neurosci. 2009 Jul;12(7):913-8
19525943
Cereb Cortex. 2003 May;13(5):435-43
12679290
Psychopharmacology (Berl). 2004 Jun;174(1):3-16
15118803
Neuron. 1993 Feb;10(2):115-25
8094962
Cereb Cortex. 2007 Oct;17(10):2443-52
17220510
Nature. 1995 Jul 6;376(6535):33-6
7596429