Causal Interactions between Frontal(θ) - Parieto-Occipital(α2) Predict Performance on a Mental Arithmetic Task.
Many neuroimaging studies have demonstrated the different functional contributions of spatially distinct brain areas to working memory (WM) subsystems in cognitive tasks that demand both local information processing and interregional coordination. In WM cognitive task paradigms employing electroencephalography (EEG), brain rhythms such as θ and α have been linked to specific functional roles over given brain areas, but their functional coupling has not been extensively studied. Here we analyzed an arithmetic task with five cognitive workload levels (CWLs) and demonstrated functional/effective coupling between the two WM subsystems: the central executive located over frontal (F) brain areas that oscillates on the dominant θ rhythm (Frontal(θ)/F(θ)) and the storage buffer located over parieto-occipital (PO) brain areas that operates on the α2 dominant brain rhythm (Parieto-Occipital(α2)/PO(α2)). We focused on important differences between and within WM subsystems in relation to behavioral performance. A repertoire of brain connectivity estimators was employed to elucidate the distinct roles of amplitude, phase within and between frequencies, and the hierarchical role of functionally specialized brain areas related to the task. Specifically, for each CWL, we conducted a) a conventional signal power analysis within both frequency bands at F(θ) and PO(α2), b) the intra- and inter-frequency phase interactions between F(θ) and PO(α2), and c) their causal phase and amplitude relationship. We found no significant statistical difference of signal power or phase interactions between correct and wrong answers. Interestingly, the study of causal interactions between F(θ) and PO(α2) revealed frontal brain region(s) as the leader, while the strength differentiated between correct and wrong responses in every CWL with absolute accuracy. Additionally, zero time-lag between bilateral F(θ) and right PO(a2) could serve as an indicator of mental calculation failure. Overall, our study highlights the significant role of coordinated activity between F(θ) and PO(α2) via their causal interactions and the timing for arithmetic performance.
Institute of Psychological Medicine and Clinical Neurosciences, Cardiff University School of MedicineCardiff, UK; Cardiff University Brain Research Imaging Center, School of Psychology, Cardiff UniversityCardiff, UK; Artificial Intelligence and Information Analysis Laboratory, Department of Informatics, Aristotle University of ThessalonikiThessaloniki, Greece; Neuroinformatics.Group, Department of Informatics, Aristotle University of ThessalonikiThessaloniki, Greece.
Stavros I
SI
Dimitriadis
Singapore Institute for Neurotechnology, Centre for Life Sciences, National University of Singapore Singapore, Singapore.
Yu
Y
Sun
Singapore Institute for Neurotechnology, Centre for Life Sciences, National University of Singapore Singapore, Singapore.
Nitish V
NV
Thakor
Singapore Institute for Neurotechnology, Centre for Life Sciences, National University of Singapore Singapore, Singapore.
Anastasios
A
Bezerianos
cognition; cross-frequency coupling; hierarchical organization; mental arithmetic; working memory
J Cogn Neurosci. 2005 Sep;17(9):1367-75
16197690
Neuroimage. 2015 Sep;118:79-89
26067344
Nat Rev Neurosci. 2001 Apr;2(4):229-39
11283746
Cereb Cortex. 2008 Aug;18(8):1788-98
18042643
Cogn Affect Behav Neurosci. 2003 Dec;3(4):255-74
15040547
J Neurosci Methods. 2010 Oct 30;193(1):145-55
20817039
Ann N Y Acad Sci. 2007 Feb;1097:67-83
17413013
Cereb Cortex. 2007 Feb;17(2):391-9
16525126
Neuroimage. 2009 Feb 1;44(3):1103-12
19027075
Neurosci Res. 1996 Sep;26(1):79-81
8895895
J Neurosci Methods. 2008 Mar 15;168(2):494-9
18061683
Nat Neurosci. 2011 May;14(5):656-61
21441920
Ergonomics. 1998 May;41(5):678-88
9613228
Annu Rev Psychol. 2015 Jan 3;66:115-42
25251486
Exp Brain Res. 2009 Jun;195(4):635-42
19452143
Front Hum Neurosci. 2010 Oct 19;4:191
21060716
Int J Psychophysiol. 2016 Apr;102:1-11
26910049
Trends Cogn Sci. 2014 Jan;18(1):16-25
24268290
Trends Cogn Sci. 2005 Oct;9(10):474-80
16150631
Electroencephalogr Clin Neurophysiol. 1972 Jul;33(1):71-80
4113276
Cogn Neuropsychol. 2003 May 1;20(3):487-506
20957581
Neuroimage. 2013 Feb 1;66:642-7
23142278
Neuroimage. 2004 Jul;22(3):1157-72
15219588
Annu Rev Neurosci. 2004;27:611-47
15217345
IEEE Trans Neural Syst Rehabil Eng. 2016 Oct;24(10 ):1017-1028
26780815
Neurobiol Learn Mem. 2009 Feb;91(2):155-65
18848635
Nat Neurosci. 2003 Jan;6(1):75-81
12469132
Annu Rev Neurosci. 1995;18:193-222
7605061
Neuroimage. 2003 Aug;19(4):1273-302
12948688
J Neurosurg. 2013 Nov;119(5):1107-11
23930858
Nat Rev Neurosci. 2002 Mar;3(3):201-15
11994752
Nature. 2004 Apr 15;428(6984):751-4
15085133
Neuroreport. 2004 Jun 7;15(8):1233-8
15167540
Trends Neurosci. 2006 Jun;29(6):317-22
16697058
Cortex. 1997 Jun;33(2):219-50
9220256
Neuroimage. 2015 Feb 1;106:144-53
25463464
Cereb Cortex. 1997 Dec;7(8):768-78
9408041
PLoS Biol. 2014 Aug 26;12(8):e1001936
25157678
Neuron. 2005 Nov 23;48(4):535-8
16301170
J Neurosci. 2007 Oct 31;27(44):11949-59
17978035
Neuroscience. 2006 Apr 28;139(1):201-8
16324792
Neuroimage. 2008 Aug 1;42(1):272-84
18515149
Hum Brain Mapp. 2009 Jun;30(6):1857-65
19235884
J Neurosci Methods. 2010 Aug 30;191(2):191-200
20600317
Springerplus. 2013 Dec;2(1):14
23440395
Cereb Cortex. 2014 Apr;24(4):1045-53
23236202
Brain Connect. 2011;1(1):13-36
22432952
Trends Cogn Sci. 2000 Jun;4(6):215-222
10827444
Comput Biol Med. 2008 Mar;38(3):348-60
18222418
PLoS Biol. 2007 Jan;5(1):e12
17199410
Cereb Cortex. 2014 Sep;24(9):2409-20
23588186
J Neurosci. 2001 Oct 15;21(20):RC177
11588207
Eur J Neurosci. 2002 Apr;15(8):1395-9
11994134
Neuroscience. 2006 Apr 28;139(1):23-38
16324795
Brain Cogn. 2012 Oct;80(1):45-52
22626921
J Neurosci. 2005 Apr 13;25(15):3962-72
15829648
Neuroimage. 2004;23 Suppl 1:S264-74
15501096
Brain Res. 2007 Oct 3;1172:93-102
17822681
Eur J Neurosci. 2010 May;31(9):1683-9
20525081
Annu Rev Neurosci. 2001;24:167-202
11283309
Nat Rev Neurosci. 2011 Feb;12(2):105-18
21248789
Front Hum Neurosci. 2016 Apr 26;10:163
27199698
Neuropsychologia. 2011 May;49(6):1407-9
21295047
Psychon Bull Rev. 2002 Dec;9(4):637-71
12613671
Cogn Neurodyn. 2015 Aug;9(4):371-87
26157511
J Neurosci Methods. 2004 Mar 15;134(1):9-21
15102499
Trends Cogn Sci. 2003 Sep;7(9):415-423
12963473
Science. 2000 Jun 2;288(5471):1656-60
10834847
Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12959-64
10536030
Neuroimage. 2006 May 1;30(4):1255-72
16473023
Neuroimage. 2009 Feb 1;44(3):796-811
19000769
Neuroimage Clin. 2015 Sep 21;9:519-31
26640764
Nat Neurosci. 2013 Oct;16(10):1484-91
23995071
Neurosci Biobehav Rev. 2006;30(6):808-22
16904745
Front Hum Neurosci. 2014 Jun 11;8:406
24966825
Neuroimage. 2007 Sep 1;37(3):706-20
17632015
Int J Psychophysiol. 2005 Aug;57(2):97-103
15967528
Cereb Cortex. 2013 Feb;23(2):389-98
22345353
Neuroimage. 2000 Oct;12(4):357-65
10988030
Science. 1999 Mar 12;283(5408):1657-61
10073923
Neurosci Lett. 1999 Oct 15;274(1):29-32
10530512
Front Neurosci. 2015 Oct 20;9:350
26539070
Neuroimage. 2006 May 1;30(4):1273-84
16490364
Brain Res Brain Res Rev. 1999 Apr;29(2-3):169-95
10209231
Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):4230-5
21368109
Brain Res. 2008 Oct 15;1235:31-44
18625208
Hum Brain Mapp. 1999;8(4):194-208
10619414
Cereb Cortex. 2001 Apr;11(4):350-9
11278198
Front Behav Neurosci. 2014 Dec 05;8:420
25538585
Neuroimage. 2012 Sep;62(3):1415-28
22634858
J Neurosci Methods. 2014 Feb 15;223:50-68
24200508
Nature. 1997 Apr 10;386(6625):604-8
9121583
Ann Biomed Eng. 2015 Apr;43(4):977-89
25287648
Annu Rev Psychol. 2013;64:499-525
22804773
J Cogn Neurosci. 1999 Nov;11(6):617-30
10601743
J Cogn Neurosci. 2011 Jan;23(1):1-10
20586702
Neuron. 2004 Mar 25;41(6):983-93
15046729
Neuropsychologia. 2006;44(6):860-8
16260006
Nature. 2004 Apr 15;428(6984):748-51
15085132
J Cogn Neurosci. 1992 Summer;4(3):281-8
23964884
Biol Cybern. 2001 Aug;85(2):145-57
11508777
Proc Natl Acad Sci U S A. 2010 Mar 16;107(11):5248-53
20194767
Neuroimage. 2011 Sep 15;58(2):312-22
19961941
Nat Rev Neurosci. 2005 Jun;6(6):435-48
15928716
Trends Cogn Sci. 2012 Apr;16(4):219-30
22440830
Curr Opin Neurobiol. 2004 Apr;14(2):218-24
15082328
Conf Proc IEEE Eng Med Biol Soc. 2013;2013:2940-3
24110343
Proc Natl Acad Sci U S A. 2011 Oct 18;108(42):17510-5
21987824
Biol Psychol. 2011 Apr;87(1):128-36
21382434
Neurosci Lett. 2007 Jul 11;422(2):141-5
17602835
Brain Res Cogn Brain Res. 2005 Mar;22(3):397-405
15722210
Neurosci Lett. 2005 Jan 20;373(3):212-7
15619545