title: Neural chronometry and coherency across speed-accuracy demands reveal lack of homomorphism between computational and neural mechanisms of evidence accumulation.
abstract: The stochastic accumulation framework provides a mechanistic, quantitative account of perceptual decision-making and how task performance changes with experimental manipulations. Importantly, it provides an elegant account of the speed-accuracy trade-off (SAT), which has long been the litmus test for decision models, and also mimics the activity of single neurons in several key respects. Recently, we developed a paradigm whereby macaque monkeys trade speed for accuracy on cue during visual search task. Single-unit activity in frontal eye field (FEF) was not homomorphic with the architecture of models, demonstrating that stochastic accumulators are an incomplete description of neural activity under SAT. This paper summarizes and extends this work, further demonstrating that the SAT leads to extensive, widespread changes in brain activity never before predicted. We will begin by reviewing our recently published work that establishes how spiking activity in FEF accomplishes SAT. Next, we provide two important extensions of this work. First, we report a new chronometric analysis suggesting that increases in perceptual gain with speed stress are evident in FEF synaptic input, implicating afferent sensory-processing sources. Second, we report a new analysis demonstrating selective influence of SAT on frequency coupling between FEF neurons and local field potentials. None of these observations correspond to the mechanics of current accumulator models.
authors.affiliation: Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Department of Psychology, Vanderbilt University, , PMB 407817, 2301 Vanderbilt Place, Nashville, TN 37240-781, USA.
authors.forename: Richard P
authors.initials: RP
authors.lastname: Heitz
authors.forename: Jeffrey D
authors.initials: JD
authors.lastname: Schall
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D002909:Chronobiology Phenomena / Q000502:physiology*; D003657:Decision Making / Q000502:physiology*; D005133:Eye Movements / Q000502:physiology*; D008251:Macaca; D008959:Models, Neurological; D010364:Pattern Recognition, Visual / Q000502:physiology*; D013045:Species Specificity; D013269:Stochastic Processes; D014794:Visual Fields / Q000502:physiology*
keywords: computational models; frontal eye field; perceptual decision-making; speed–accuracy trade-off; visual attention; visual search
references.citation: PLoS One. 2008 Jul 09;3(7):e2635
references.pmid: 18612380
references.citation: J Neurosci. 2010 Nov 24;30(47):15747-59
references.pmid: 21106814
references.citation: Psychol Sci. 2008 Feb;19(2):128-36
references.pmid: 18271860
references.citation: Neural Comput. 2001 Apr;13(4):717-49
references.pmid: 11255566
references.citation: Front Psychol. 2012 Aug 01;3:263
references.pmid: 22870070
references.citation: Nat Neurosci. 2000 Aug;3(8):827-30
references.pmid: 10903577
references.citation: Trends Cogn Sci. 2005 Oct;9(10):474-80
references.pmid: 16150631
references.citation: J Neurosci. 2006 Mar 1;26(9):2487-98
references.pmid: 16510727
references.citation: Psychol Rev. 1997 Apr;104(2):266-300
references.pmid: 9127583
references.citation: Proc Natl Acad Sci U S A. 2010 Sep 7;107(36):15916-20
references.pmid: 20733082
references.citation: Electroencephalogr Clin Neurophysiol. 1996 Sep;99(3):225-34
references.pmid: 8862112
references.citation: J Neurosci. 2011 Jul 20;31(29):10627-39
references.pmid: 21775606
references.citation: Science. 2012 Oct 5;338(6103):132-5
references.pmid: 23042897
references.citation: Psychol Rev. 2005 Apr;112(2):291-328
references.pmid: 15783288
references.citation: Cereb Cortex. 2000 Dec;10(12):1233-41
references.pmid: 11073872
references.citation: Eur J Neurosci. 2011 Jun;33(11):2003-16
references.pmid: 21645096
references.citation: Nat Rev Neurosci. 2001 Oct;2(10):704-16
references.pmid: 11584308
references.citation: J Neurosci. 2013 Feb 6;33(6):2254-67
references.pmid: 23392657
references.citation: Trends Neurosci. 2009 Jan;32(1):9-18
references.pmid: 19012975
references.citation: Nature. 2004 Oct 14;431(7010):859-62
references.pmid: 15483614
references.citation: J Neurophysiol. 2005 Jan;93(1):337-51
references.pmid: 15317836
references.citation: PLoS Biol. 2008 Jul 1;6(7):e158
references.pmid: 18656991
references.citation: Proc Natl Acad Sci U S A. 2009 Apr 21;106(16):6539-44
references.pmid: 19342495
references.citation: J Comp Neurol. 1988 May 22;271(4):493-506
references.pmid: 2454971
references.citation: J Neurophysiol. 1996 Dec;76(6):4040-55
references.pmid: 8985899
references.citation: Neuron. 2003 May 22;38(4):637-48
references.pmid: 12765614
references.citation: Science. 2007 Mar 30;315(5820):1860-2
references.pmid: 17395832
references.citation: Science. 2003 Jan 3;299(5603):81-6
references.pmid: 12511644
references.citation: Neural Netw. 2006 Oct;19(8):1013-26
references.pmid: 16987636
references.citation: J Neurophysiol. 2006 May;95(5):3277-80
references.pmid: 16436477
references.citation: Psychophysiology. 1998 Jan;35(1):99-115
references.pmid: 9499711
references.citation: J Neurosci Methods. 2007 Jun 15;163(1):161-75
references.pmid: 17395267
references.citation: Cogn Affect Behav Neurosci. 2007 Dec;7(4):396-412
references.pmid: 18189013
references.citation: Psychophysiology. 1994 May;31(3):291-308
references.pmid: 8008793
references.citation: J Neurophysiol. 2009 Apr;101(4):1699-704
references.pmid: 19176607
references.citation: J Neurophysiol. 1999 Sep;82(3):1198-208
references.pmid: 10482739
references.citation: J Neurosci. 2009 Dec 16;29(50):15621-9
references.pmid: 20016076
references.citation: Annu Rev Neurosci. 1995;18:193-222
references.pmid: 7605061
references.citation: J Neurophysiol. 2009 May;101(5):2485-506
references.pmid: 19261711
references.citation: J Exp Psychol Hum Percept Perform. 1990 Aug;16(3):459-78
references.pmid: 2144564
references.citation: Psychon Bull Rev. 2002 Jun;9(2):278-91
references.pmid: 12120790
references.citation: J Neurosci. 2008 Mar 19;28(12):2991-3007
references.pmid: 18354003
references.citation: Trends Neurosci. 2010 Jan;33(1):10-6
references.pmid: 19819033
references.citation: Nat Neurosci. 2012 Dec;15(12):1729-35
references.pmid: 23103963
references.citation: J Neurosci. 2002 Nov 1;22(21):9475-89
references.pmid: 12417672
references.citation: Curr Opin Neurobiol. 2012 Dec;22(6):1012-21
references.pmid: 22749788
references.citation: J Neurophysiol. 1998 Feb;79(2):817-34
references.pmid: 9463444
references.citation: J Neurophysiol. 2010 Nov;104(5):2433-41
references.pmid: 20810692
references.citation: Exp Brain Res. 2008 Sep;190(2):135-51
references.pmid: 18604527
references.citation: Science. 1996 Oct 18;274(5286):427-30
references.pmid: 8832893
references.citation: J Neurosci. 2012 Mar 7;32(10):3433-46
references.pmid: 22399766
references.citation: Psychon Bull Rev. 1994 Jun;1(2):202-38
references.pmid: 24203471
references.citation: J Neurosci. 2000 Jan 1;20(1):387-400
references.pmid: 10627615
references.citation: Cereb Cortex. 2003 Nov;13(11):1257-69
references.pmid: 14576217
references.citation: J Neurophysiol. 2003 Sep;90(3):1392-407
references.pmid: 12761282
references.citation: J Neurosci. 2011 Nov 30;31(48):17488-95
references.pmid: 22131410
references.citation: Psychol Rev. 2010 Oct;117(4):1113-43
references.pmid: 20822291
references.citation: Psychol Rev. 2006 Oct;113(4):700-65
references.pmid: 17014301
references.citation: J Neurosci. 2005 Nov 9;25(45):10420-36
references.pmid: 16280581
references.citation: Science. 2009 May 29;324(5931):1207-10
references.pmid: 19478185
references.citation: J Comp Neurol. 1986 Nov 22;253(4):415-39
references.pmid: 3793998
references.citation: J Neurophysiol. 1976 Jul;39(4):745-65
references.pmid: 823303
references.citation: J Vis. 2005 May 02;5(5):376-404
references.pmid: 16097871
references.citation: Psychol Rev. 2004 Apr;111(2):333-67
references.pmid: 15065913
references.citation: J Exp Psychol Gen. 2004 Jun;133(2):261-82
references.pmid: 15149253
references.citation: Trends Cogn Sci. 2006 Aug;10(8):382-90
references.pmid: 16843702
references.citation: J Neurosci. 2003 Jul 23;23(16):6480-9
references.pmid: 12878689
references.citation: Nature. 1999 Aug 26;400(6747):867-9
references.pmid: 10476964
references.citation: Electroencephalogr Clin Neurophysiol Suppl. 1999;52:3-6
references.pmid: 10590970
references.citation: J Neurosci. 1999 Apr 1;19(7):2740-54
references.pmid: 10087086
references.citation: Science. 2005 Apr 22;308(5721):529-34
references.pmid: 15845848
references.citation: Prog Brain Res. 2005;147:251-62
references.pmid: 15581711
references.citation: Science. 2001 Feb 23;291(5508):1560-3
references.pmid: 11222864
references.citation: Nat Neurosci. 1999 Feb;2(2):176-85
references.pmid: 10195203
references.citation: J Neurophysiol. 1977 Jul;40(4):861-78
references.pmid: 407334
references.citation: Trends Cogn Sci. 2007 Mar;11(3):118-25
references.pmid: 17276130
references.citation: Nature. 2006 Feb 9;439(7077):733-6
references.pmid: 16372022
references.citation: J Neurophysiol. 2003 Nov;90(5):3538-46
references.pmid: 12815017
references.citation: Neuron. 2008 Feb 28;57(4):614-25
references.pmid: 18304489
references.citation: Exp Brain Res. 2002 Feb;142(4):439-62
references.pmid: 11845241
references.citation: Cogn Psychol. 2008 Nov;57(3):153-78
references.pmid: 18243170
references.citation: J Cogn Neurosci. 2008 Nov;20(11):1952-65
references.pmid: 18416686
references.citation: Annu Rev Physiol. 2004;66:735-69
references.pmid: 14977420
references.citation: J Neurophysiol. 2009 Oct;102(4):2375-86
references.pmid: 19675287
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 18;104(38):15111-6
references.pmid: 17848520
references.citation: J Neurophysiol. 1985 Mar;53(3):603-35
references.pmid: 3981231
references.citation: J Neurosci. 2010 Apr 21;30(16):5498-507
references.pmid: 20410103
references.citation: PLoS One. 2011 Jan 21;6(1):e16276
references.pmid: 21283699
references.citation: J Exp Psychol Learn Mem Cogn. 1992 Sep;18(5):883-914
references.pmid: 1402715
references.citation: Nature. 1998 Jan 29;391(6666):481-4
references.pmid: 9461214
references.citation: Neuron. 2012 Nov 8;76(3):616-28
references.pmid: 23141072
references.citation: Neuron. 2005 Mar 3;45(5):801-14
references.pmid: 15748854
references.citation: Front Neuroanat. 2009 May 22;3:2
references.pmid: 19506705
references.citation: Psychol Rev. 2001 Jul;108(3):550-92
references.pmid: 11488378
references.citation: Front Comput Neurosci. 2011 Feb 11;5:7
references.pmid: 21415911
references.citation: J Neurophysiol. 2007 Feb;97(2):1756-74
references.pmid: 17122324
references.citation: J Neurophysiol. 1992 Dec;68(6):1967-85
references.pmid: 1491252
references.citation: Cereb Cortex. 2012 May;22(5):1052-67
references.pmid: 21765183
references.citation: J Neurosci. 2011 Jan 26;31(4):1254-66
references.pmid: 21273410
references.citation: Psychol Rev. 2007 Apr;114(2):376-97
references.pmid: 17500631
references.citation: Neuron. 2009 Jan 15;61(1):35-41
references.pmid: 19146811
references.citation: Nat Neurosci. 2006 Jul;9(7):948-55
references.pmid: 16751764
references.citation: Proc Natl Acad Sci U S A. 2008 Nov 11;105(45):17538-42
references.pmid: 18981414
references.citation: Science. 2008 Apr 4;320(5872):110-3
references.pmid: 18388295
references.citation: Nat Neurosci. 2008 Jun;11(6):693-702
references.pmid: 18488024