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Neuroscience Bulletin logoLink to Neuroscience Bulletin
. 2013 Apr 18;29(3):279–286. doi: 10.1007/s12264-013-1333-z

Encoding of rat working memory by power of multi-channel local field potentials via sparse non-negative matrix factorization

Xu Liu 11333, Tiao-Tiao Liu 21333, Wen-Wen Bai 21333, Hu Yi 21333, Shuang-Yan Li 11333, Xin Tian 11333,21333,
PMCID: PMC5561844  PMID: 23606209

Abstract

Working memory plays an important role in human cognition. This study investigated how working memory was encoded by the power of multi-channel local field potentials (LFPs) based on sparse nonnegative matrix factorization (SNMF). SNMF was used to extract features from LFPs recorded from the prefrontal cortex of four Sprague-Dawley rats during a memory task in a Y maze, with 10 trials for each rat. Then the power-increased LFP components were selected as working memory-related features and the other components were removed. After that, the inverse operation of SNMF was used to study the encoding of working memory in the time-frequency domain. We demonstrated that theta and gamma power increased significantly during the working memory task. The results suggested that postsynaptic activity was simulated well by the sparse activity model. The theta and gamma bands were meaningful for encoding working memory.

Keywords: sparse non-negative matrix factorization, multi-channel local field potentials, working memory, prefrontal cortex

References

  • [1].Mintzer MZ, Griffiths RR. Differential effects of scopolamine and lorazepam on working memory maintenance versus manipulation processes. Cogn Affect Behav Neurosci. 2007;7:120–129. doi: 10.3758/CABN.7.2.120. [DOI] [PubMed] [Google Scholar]
  • [2].Baddeley AD. Working memory: looking back and looking forward. Nat Rev Neurosci. 2003;4:829–839. doi: 10.1038/nrn1201. [DOI] [PubMed] [Google Scholar]
  • [3].Lupien SJ, Buss C, Schramek TE. Hormetic influence of glucocorticoids on human memory. Nonlinearity Biol Toxicol Med. 2005;3:23–56. doi: 10.2201/nonlin.003.01.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [4].Miller EK. An integrative theory of prefrontal cortex. Ann Rev Neurosci. 2001;24:167–202. doi: 10.1146/annurev.neuro.24.1.167. [DOI] [PubMed] [Google Scholar]
  • [5].Wang XJ. Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci. 2001;24:455–463. doi: 10.1016/S0166-2236(00)01868-3. [DOI] [PubMed] [Google Scholar]
  • [6].Fuster JM, Bauer RH, Jervey J. Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Res. 1985;330:299–307. doi: 10.1016/0006-8993(85)90689-4. [DOI] [PubMed] [Google Scholar]
  • [7].Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC. A parametric study of prefrontal cortex involvement in human working memory. Neuroimage. 1997;5:49–62. doi: 10.1006/nimg.1996.0247. [DOI] [PubMed] [Google Scholar]
  • [8].Logothetis NK. The underpinnings of the BOLD functional magnetic resonance imaging signal. J Neurosci. 2003;23:3963–3971. doi: 10.1523/JNEUROSCI.23-10-03963.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [9].Pesaran B, Pezaris J, Sahani M, Mitra PP, Andersen RA. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci. 2002;5:805–811. doi: 10.1038/nn890. [DOI] [PubMed] [Google Scholar]
  • [10].Carsten M, Jörn R, Eilon V, Oliveira SC, Aertsen A, Rotter S. Inference of hand movements from local field potentials in monkey motor cortex. Nat Neurosci. 2003;6:1253–1254. doi: 10.1038/nn1158. [DOI] [PubMed] [Google Scholar]
  • [11].Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, et al. Coherent theta oscillations and reorganization of spike timing in the hippocampalprefrontal network upon learning. Neuron. 2010;66:921–936. doi: 10.1016/j.neuron.2010.05.013. [DOI] [PubMed] [Google Scholar]
  • [12].Montgomery SM, Buzsaki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci U S A. 2007;104:14495–14500. doi: 10.1073/pnas.0701826104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [13].Driver JE, Racca C, Cunningham MO, Towers SK, Davies CH, Whittington MA, et al. Impairment of hippocampal gamma-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP) Eur J Neurosci. 2007;26:1280–1288. doi: 10.1111/j.1460-9568.2007.05705.x. [DOI] [PubMed] [Google Scholar]
  • [14].Lisman J. The theta/gamma discrete code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus. 2005;15:913–922. doi: 10.1002/hipo.20121. [DOI] [PubMed] [Google Scholar]
  • [15].Histed MH, Bonin V, Reid RC. Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron. 2009;63:508–522. doi: 10.1016/j.neuron.2009.07.016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [16].Joelving FC, Compte A, Constantinidis C. Temporal properties of posterior parietal neuron discharges during working memory and passive viewing. J Neurophysiol. 2007;97:2254–2266. doi: 10.1152/jn.00977.2006. [DOI] [PubMed] [Google Scholar]
  • [17].Lundqvist M, Herman P, Lansner A. Theta and Gamma power increases and Alpha/Beta power decreases with memory load in an attractor network model. J Cogn Neurosci. 2011;23:3008–3020. doi: 10.1162/jocn_a_00029. [DOI] [PubMed] [Google Scholar]
  • [18].Siegel M, Warden MR, Miller EK. Phase-dependent neuronal coding of objects in short-term memory. Proc Natl Acad Sci U S A. 2009;106:21341–21346. doi: 10.1073/pnas.0908193106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [19].Fujisawa S, Buzsáki G. A 4 Hz oscillation adaptively synchronizes prefrontal, vta, and hippocampal activities. Neuron. 2011;72:153–165. doi: 10.1016/j.neuron.2011.08.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [20].Olshausen BA, Field DJ. Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature. 1996;381:607–609. doi: 10.1038/381607a0. [DOI] [PubMed] [Google Scholar]
  • [21].Kim H, Park H. Sparse non-negative matrix factorizations via alternating non-negativity-constrained least squares for microarray data analysis. Bioinformatics. 2007;23:1495–1502. doi: 10.1093/bioinformatics/btm134. [DOI] [PubMed] [Google Scholar]
  • [22].Hoyer PO. Nonnegative matrix factorization with sparseness constraints. J Mach Learn Res. 2004;5:1457–1469. [Google Scholar]
  • [23].Lee DD, Seung HS. Algorithms for non-negative matrix factorization. Adv Neural Inf Process Syst. 2001;13:556–562. [Google Scholar]
  • [24].Shi JL, Luo ZG. Research on the Advances of nonnegative matrix factorization and its application in bioinformatics. Comput Eng Sci. 2010;32:117–123. [Google Scholar]
  • [25].Kim PM, Tidor B. Subsystem identification through dimensionality reduction of large-scale gene expression data. Genome Res. 2003;13:1706–1718. doi: 10.1101/gr.903503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [26].Monti S, Tamayo P, Mesirov J, Golub T. Consensus clustering: A resampling based method for class discovery and visualization of gene expression microarray data. Mach Learn. 2003;52:91–118. doi: 10.1023/A:1023949509487. [DOI] [Google Scholar]
  • [27].Hazan T, Polak S, Shashua A. Sparse image coding using a 3D nonnegative tensor factorization. IEEE ICCV. 2005;1:50–57. [Google Scholar]
  • [28].Raqhavachari S, Lisman JE, Tully M, Madsen JR, Bromfield EB, Kahana MJ. Theta oscillations in human cortex during a working-memory task: evidence for local generators. J Neurophysiol. 2006;95:1630–1638. doi: 10.1152/jn.00409.2005. [DOI] [PubMed] [Google Scholar]
  • [29].Missonnier P, Gold G, Herrmann FR, Fazio-Costa L, Michel JP, Deiber MP, et al. Decreased theta eventrelated synchronization during working memory activation is associated with progressive mild cognitive impairment. Dement Geriatr Cogn Disord. 2006;22:250–259. doi: 10.1159/000094974. [DOI] [PubMed] [Google Scholar]
  • [30].Hyman JM, Hasselmo ME, Seaman JK. What is the functional relevance of prefrontal cortex entrainment to hippocampal theta rhythms? Front Neurosci. 2011;5:24. doi: 10.3389/fnins.2011.00024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [31].Jones MW, Wilson MA. Theta rhythms coordinate hippocampal — prefrontal interactions in a spatial memory task. PLoS Biol. 2005;3:2187–2199. doi: 10.1371/journal.pbio.0030402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [32].Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, et al. Gating of human theta oscillations by a working memory task. J Neurosci. 2001;21:3175–3183. doi: 10.1523/JNEUROSCI.21-09-03175.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [33].Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, et al. Gamma oscillations correlate with working memory load in humans. Cereb Cortex. 2003;13:1369–1374. doi: 10.1093/cercor/bhg084. [DOI] [PubMed] [Google Scholar]
  • [34].Herrmann CS, Munk MH, Engel AK. Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn Sci. 2004;8:347–355. doi: 10.1016/j.tics.2004.06.006. [DOI] [PubMed] [Google Scholar]
  • [35].Sejnowski TJ, Destexhe A. Why do we sleep? Brain Res. 2000;886:208–223. doi: 10.1016/S0006-8993(00)03007-9. [DOI] [PubMed] [Google Scholar]
  • [36].Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, et al. High gamma power is phase locked to theta oscillations in human neocortex. Science. 2006;313:1626–1628. doi: 10.1126/science.1128115. [DOI] [PMC free article] [PubMed] [Google Scholar]

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