{"title": "Independent Component Analysis of Electroencephalographic Data", "book": "Advances in Neural Information Processing Systems", "page_first": 145, "page_last": 151, "abstract": null, "full_text": "Independent  Component  Analysis \nof Electroencephalographic Data \n\nScott  Makeig \n\nNaval  Health  Research  Center \n\nP.O.  Box 85122 \n\nSan  Diego CA  92186-5122 \n\nAnthony J.  Bell \n\nComputational Neurobiology  Lab \nThe Salk Institute,  P.O.  Box 85800 \n\nSan Diego,  CA  92186-5800 \n\nscott~cplJmmag.nhrc.navy.mil \n\ntony~salk.edu \n\nTzyy-Ping Jung \n\nNaval  Health  Research  Center  and \nComputational Neurobiology Lab \nThe Salk Institute,  P.O.  Box  85800 \n\nSan Diego,  CA  92186-5800 \n\nTerrence J.  Sejnowski \n\nHoward  Hughes  Medical  Institute and \n\nComputational Neurobiology Lab \nThe Salk Institute,  P.O.  Box 85800 \n\nSan Diego,  CA  92186-5800 \n\njung~salk.edu \n\nterry~salk.edu \n\nAbstract \n\nBecause of the distance between the skull and brain and their differ(cid:173)\nent resistivities,  electroencephalographic (EEG) data collected from \nany  point  on  the  human scalp  includes  activity  generated  within \na  large  brain area.  This spatial smearing of EEG  data by  volume \nconduction  does  not involve significant time delays,  however,  sug(cid:173)\ngesting that the Independent  Component  Analysis (ICA) algorithm \nof Bell and Sejnowski [1]  is suitable for  performing blind source sep(cid:173)\naration on EEG data.  The ICA algorithm separates the problem of \nsource  identification from  that of source  localization.  First  results \nof applying the ICA  algorithm to  EEG and  event-related potential \n(ERP)  data  collected  during  a  sustained  auditory  detection  task \nshow:  (1)  ICA training is insensitive to different  random seeds.  (2) \nICA may be used to segregate obvious artifactual EEG components \n(line and muscle noise, eye movements) from other sources.  (3) ICA \nis  capable of isolating overlapping  EEG  phenomena,  including  al(cid:173)\npha and theta bursts and spatially-separable ERP components, to \nseparate  ICA  channels.  (4)  N onstationarities  in  EEG  and  behav(cid:173)\nioral state can be  tracked using ICA  via changes  in  the  amount of \nresidual  correlation  between  ICA-filtered  output channels. \n\n\f146 \n\nS. MAKEIG, A. l . BELL, T.-P. lUNG, T. l. SEJNOWSKI \n\n1 \n\nIntroduction \n\n1.1  Separating What from Where in EEG  Source Analysis \n\nThe joint problems of EEG  source  segregation,  identification,  and  localization are \nvery  difficult,  since  the  problem  of determining  brain  electrical  sources  from  po(cid:173)\ntential patterns  recorded  on the scalp  surface  is  mathematically underdetermined. \nRecent  efforts  to identify  EEG  sources  have  focused  mostly on  verforming spatial \nsegregation  and  localization of source  activity  [4].  By  applying the  leA algorithm \nof Bell  and Sejnowski  [1],  we  attempt to completely separate  the twin  problems of \nsource  identification  (What)  and source  localization  (Where).  The leA algorithm \nderives  independent  sources  from  highly  correlated  EEG  signals  statistically  and \nwithout  regard  to  the  physical  location  or  configuration of the source  generators. \nRather than modeling the EEG as a  unitary output of a  multidimensional dynami(cid:173)\ncal system, or as  \"the roar of the crowd\"  of independent microscopic generators, we \nsuppose  that  the  EEG  is  the  output  of a  number  of statistically  independent  but \nspatially fixed  potential-generating systems which may either be spatially restricted \nor  widely  distributed . \n\n1.2 \n\nIndependent Component  Analysis \n\nIndependent  Component Analysis  (leA)  [1,  3]  is  the  name given  to techniques  for \nfinding  a  matrix,  Wand a  vector,  w,  so  that  the  elements,  u  =  (Ul  .. . uNF,  of \nthe  linear  transform u  =  Wx + W  of the random vector,  x  =  [Xl  ... xNF,  are sta(cid:173)\ntistically  independent.  In  contrast  with  decorrelation  techniques  such  as  Principal \nComponents  Analysis  (peA)  which  ensure  that  {UiUj}  = 0, Vij,  ICA  imposes  the \nmuch stronger  criterion  that  the  multivariate probability density  function  (p .d.f.) \nof u  factorizes:  fu(u)  = n::l fu.(ud .  Finding such  a  factorization  involves  mak(cid:173)\ning  the  mutual information between  the  Ui  go  to  zero:  I(ui,uj)  =  O,Vij.  Mutual \ninformation is a measure which depends on all higher-order statistics of the Ui  while \ndecorrelation  only takes  account of 2nd-order statistics. \n\nIn  (1],  a  new  algorithm was  proposed  for  carrying out leA. The only prior assump(cid:173)\ntion is  that the unknown  independent  components, Ui,  each  have the same form  of \ncumulative density function (c.d.f.)  after scaling and shifting, and that we know this \nform,  call  it  Fu(u).  ICA  can  then  be  performed by  maximizing the entropy,  H(y), \nof a  non-linearly  transformed  vector:  y  =  Fu(u) .  This  yields  stochastic  gradient \nascent  rules  for  adjusting Wand w: \n\nwhere  y =  (:ih  ... YN F, the elements of which  are: \n\n, \nYi  =  - - whic \n\na 0Yi  (h  \n0Yi  OUi \n\nif y  =  Fu  U \n\n(  )] \n\n(1) \n\n(2) \n\n_  Ofu(Ui) \nOFu(Ui) \n\nIt can be shown that an leA solution is  a stable point of the relaxation of eqs.(1-2) . \nIn practical tests on separating mixed speech signals, good  results were  found when \nusing  the  logistic  function,  Yi  =  (1  + e- u\u2022 )-1,  instead  of the  known  c.d.f.,  Fu, of \nthe speech  signals.  In this case  Yi  =  1 - 2Yi,  and  the algorithm has a  simple form. \nThese results were obtained despite the fact that the p.d.f. of the speech signals was \nnot exactly  matched by  the gradient of the logistic function.  In the experiments in \nthis  paper,  we  also used  the speedup  technique of prewhitening described  in  [2] . \n\n\fIndependent Component  Analysis  of Electroencephalographic  Data \n\n147 \n\n1.3  Applying leA to EEG  Data \n\nThe leA technique  appears  ideally  suited  for  performing source  separation  in  do(cid:173)\nmains  where,  (1)  the  sources  are  independent,  (2)  the  propagation  delays  of the \n'mixing medium' are  negligible, (3)  the sources  are analog and have  p.d.f.'s not too \nunlike the gradient of a logistic sigmoid, and  (4)  the  number of independent  signal \nsources  is  the  same  as  the  number  of sensors,  meaning  if  we  employ  N  sensors, \nusing  the  ICA  algorithm we  can  separate  N  sources.  In  the  case  of EEG  signals, \nN  scalp  electrodes  pick  up  correlated  signals  and  we  would  like  to  know  what  ef(cid:173)\nfectively  'independent  brain sources'  generated  these  mixtures.  If we  assume  that \nthe  complexity of EEG  dynamics can  be  modeled,  at least  in  part,  as  a  collection \nof a  modest  number  of statistically  independent  brain  processes,  the  EEG  source \nanalysis  problem  satisfies  leA assumption  (1) .  Since  volume  conduction  in  brain \ntissue is effectively instantaneous, leA assumption (2)  is  also satisfied.  Assumption \n(3)  is  plausible, but assumption (4),  that the EEG  is a linear mixtures of exactly N \nsources,  is  questionable,  since  we  do  not  know  the effective  number of statistically \nindependent  brain signals  contributing  to  the  EEG  recorded  from  the  scalp.  The \nforemost  problem  in  interpreting the  output of leA is,  therefore,  determining the \nproper dimension of input channels,  and the physiological and/or psychophysiolog(cid:173)\nical significance of the derived  leA source  channels. \n\nAlthough the leA model of the EEG ignores the known variable synchronization of \nseparate EEG generators by common subcortical or corticocortical influences  [5],  it \nappears promising for  identifying concurrent signal sources  that are either situated \ntoo close  together, or are too widely  distributed to be separated by current localiza(cid:173)\ntion techniques.  Here,  we  report a first  application of the ICA algorithm to analysis \nof 14-channel  EEG  and  ERP  recordings  during  sustained  eyes-closed  performance \nof an auditory detection task, and give evidence suggesting that the leA algorithm \nmay be useful  for  identifying psychophysiological state transitions. \n\n2  Methods \n\nEEG  and behavioral data were  collected  to develop  a  method of objectively  moni(cid:173)\ntoring the alertness  of operators of complex systems  [8] .  Ten  adult volunteers  par(cid:173)\nticipated in three or more half-hour sessions,  during which they pushed  one button \nwhenever  they  detected  an  above-threshold  auditory  target  stimulus  (a  brief  in(cid:173)\ncrease  in the level  of the continuously-present  background  noise).  To maximize the \nchance of observing alertness decrements, sessions were conducted in a small, warm, \nand dimly-lit experimental chamber, and subjects were instructed to keep their eyes \nclosed .  Auditory  targets  were  350  ms  increases  in  the  intensity  of a  62  dB  white \nnoise background,  6 dB  above their  threshold of detectability, presented  at random \ntime intervals at a  mean rate of 10/min, and superimposed on a  continuous 39-Hz \nclick train evoking a  39-Hz  steady-state  response  (SSR).  Short, and task-irrelevant \nprobe  tones  of two  frequencies  (568  and  1098  Hz)  were  interspersed  between  the \ntarget  noise  bursts  at  2-4  s  intervals.  EEG  was  collected  from  thirteen  electrodes \nlocated at sites  of the International  10-20 System, referred  to the  right mastoid, at \na  sampling rate of 312.5  Hz.  A  bipolar  diagonal electrooculogram  (EOG)  channel \nwas  also  recorded  for  use  in  eye  movement artifact  correction  and  rejection.  Tar(cid:173)\nget  Hits were  defined  as  targets  responded  to within a  100-3000 ms window,  while \nLapses were  targets not responded  to.  Two sessions each from three of the subjects \nwere  selected  for  analysis  based  on  their  containing  at  least  50  response  Lapses. \nA  continuous performance  measure,  local  error  rate,  was  computed by  convolving \nthe  irregularly-sampled performance index time series  (Hit=O/Lapse=l)  with  a  95 \ns smoothing window  advanced  for  1.64  s  steps. \n\n\f148 \n\nS.  MAKEIG, A.  l. BELL, T.-P. lUNG, T. 1.  SEJNOWSKI \n\nThe leA algorithm in  eqs.(1-2)  was  applied  to  the  14  EEG  recordings.  The  time \nindex was permuted to ensure signal stationarity, and the 14-dimensional time point \nvectors  were  presented  to a  14  ---.  14  leA network one at a  time.  To speed  conver(cid:173)\ngence,  we  first  pre-whitened  the data to  remove  first- and  second-order  statistics. \nThe learning rate was  annealed  from 0.03 to 0.0001 during convergence.  After  each \npass through the whole training set,  we  checked the amount of correlation between \nthe leA output channels and the amount of change  in weight  matrix, and stopped \nthe training procedure  when,  (1)  the mean correlation among all channel  pairs was \nbelow  0.05, and (2)  the leA weights had stopped  changing appreciably. \n\n3  Results \n\nA small (4.5 s)  portion of the resulting  leA-transformed  EEG time series is  shown \nin Figure 1.  As expected, correlations between the leA traces are close  to zero.  The \ndominant theta wave  (near  7  Hz)  spread  across  many EEG  channels  (left  paneQ  is \nmore  or  less  isolated  to  leA  trace  1  (upper  right),  both  in  the  epoch  shown  and \nthroughout the session.  Alpha activity  (near  10  Hz)  not obvious in the  EEG  data \nis  uncovered  in leA trace 2,  which  here  and throughout the session  contains alpha \nbursts  interspersed  with  quiescent  periods.  Other  leA  traces  (3-8)  contain  brief \noscillatory  bursts  which  are  not easy  to  characterize,  but  clearly  display  different \ndynamics from  the  activity  in  leA trace  1 which  dominates the  raw  EEG  record. \nICA  trace  10  contains near-De changes associated with eye  slow  movements in the \nEOG  and  most  frontal  (Fpz)  EEG  channels.  leA  trace  13  contains  mostly  line \nnoise  (60  Hz),  while  ICA  traces  9  and  14  have  a  broader  high  frequency  (50-100 \nHz)  spectrum,  suggesting  that  their  source  is  likely  to  be  high-frequency  activity \ngenerated  by  scalp  muscles. \n\nApparently,  the  ICA  source  solution  for  this  data  does  not  depend  strongly  on \nlearning rate or initial conditions.  When the same portion of one session was used to \ntrain  two  leA networks  with  different  random starting weights,  data presentation \norders,  and  learning  rates,  the  two  final  ICA  weight  matrices  were  very  close  to \none  another.  Filtering another  segment  of EEG  data from  the  same session  using \neach  ICA  matrix produced  two ICA source  transforms in which  11  of the  14  best(cid:173)\ncorrelated output channel  pairs correlated above 0.95 and none correlated  less  than \n0.894. \n\nWhile ICA  training minimized mutual information, and therefore  also correlations \nbetween output channels during the initial (alert) leA training period, output data \nchannels  filtered  by  the  same  leA  weight  matrix  became  more  correlated  dur(cid:173)\ning  the  drowsy  portion  of the  session,  and  then  reverted  to  their  initial  levels  of \n(de)correlation when the subject  again became alert.  Conversely, filtering the same \nsession's  data with an leA weight  matrix trained on  the drowsy  portion of the ses(cid:173)\nsion  produced  output channels that were  more correlated  during the alert portions \nof the session  than during  the  drowsy  training  period.  Presumably, these  changes \nin  residual  correlation  among  ICA  outputs  reflect  changes  in  the  dynamics  and \ntopographic structure of the  EEG signals in alert  and  drowsy  brain states. \n\nAn important problem in human electrophysiology is to determine a means of objec(cid:173)\ntively identifying overlapping ERP subcomponents.  Figure 3 (right paneQ  shows an \nleA decomposition of (left  paneQ  ERPs to detected  (Hit)  and  undetected  (Lapse) \ntargets  by  the  same subject.  leA spatial filtering  produces  two  channels  (S[I-2]) \nseparating out the  39-Hz  steady-state  response  (SSR)  produced  by  the  continuous \n39-Hz  click  stimulation  during  the  session.  Note  the  stimulus-induced  perturba(cid:173)\ntion  in  SSR  amplitude previously  identified  in \n[6] .  Three  channels  (H[I-3])  pass \ntime-limited components of the  detected  target response,  while four  others  (1[1-4]) \n\n\fIndependent  Component  Analysis  of Electroencephalographic  Data \n\nJ 49 \n\nEEG \n\nleA \n\nFz  ~V~~~hI'o/A. \nCz  ~~MvN'N{\\~v<wv'yJ\\J\\r\"~ \n\npz  V&V\\fM~IIjJ-r~ \n\n3 VfJV\\.'\\I\\~~~'~ \n4  'rIvV\\.JJvvV'-r~\u00b7~, \n\nF3  .;vwvwvvvrv~~WV'JI~ \n\n5 i~'MI'\\'V1fV{\\tNN~10~~ \n\nF4  ~\\0.,fvo/lf'1Vlf\\,~~~ \n\n6  {.I'VVVVVvw....;;~~rwvr'ri(.,'r\u00b7Nvf \n\nC3  VIV\"'vVWv!l!vWN/W\\'~~ \n\n7  /<\u00a5Yl1~'riiwNV~~~~ \n\nC4  \\MIV{lAtv!ifVV{\\AfJV0~~ \n\n8  ~v.AJvJw-~\\Jn~ \n\n9 >I*~vw~Y!\"'~.fW'Iwi'fr.\"'I \n\nT4 ~~~~ \n\n10 ~~~~~ \n\nP3  v\"V'v\"\"Nv\\~\"'-'V \n\n11  1~IVVV~\\fvv{iJYlw~~ \n\nP4  M'-VVI/<{WY'V0,Ww~ \nFpz  ~\\~I\"IVlV';.~~ \nEOG~~~ \n\n12/\u00a5v\\~~ \n\n13~~~~~~~ \n\n14  ~~\\\"W!~~~~~ \n\n- - 1 sec. \n\nFigure  1:  Left:  4.5  seconds  of 14-channel  EEG  data.  Right :  an  l e A  transform  of \nthe same data, using  weights  trained  on  6.5  minutes of similar data from the same \nseSSlOn. \n\n\f150 \n\nS.  MAKEIG, A. J. BELL, T.-P. JUNG, T. J.  SEJNOWSKI \n\nScalp ERPs \n\nICAERPs \n\nFz  ~~~~...., \n\nCz \n\npz \n\nOz \n\n+ \n;.,  ~~P \u2022. ..-.woiQfiS$i \n-... + \"-,;r::> Gtr~ --,.~ \n+ \n+ \n~ .,. \n+ \n\n,  Q  . . .   \u00a2I,;;\"  '''iIi  04\"'. \n\nF4 \n\nC3 \n\n+ \n\n....  '''''''S \n\nF3  ~ \"\"~~n;; \n:1 ~;f'O\"IV'~~ 'tV; \n+ \n-., '  1;so~ ;  _ \n+ \n;;., ,~, coA'C>\"\",~ .... ,W Ii ::v; \n+ \n~ 1\"\u00b7\" ,,~\"\" ~;t;!\u00a5 ;Nft~h'\" \n+ \n;'+~~t ~~~.\"w \n+ - .J \n1  c ......... r::c;.,.~4&f'  !  c  44c;c;e \n\nP3 \n\nC4 \n\nT3 \n\nT4 \n\n+ \n~.\"  0\u00ab  '4  ~~;. '\" \n+ \n\nP4 \n\n\u2022 j\"  \"\"*+ \n\n+ \n\nFPZ~n~~~ \u2022. \nEOG;\"\"1 \n+ \no \n\n... ~ ...  '1* \n0.6 \n\n::  -.........-\n\nit~ \n1 sec \n\n0.2 \n\n0.8 \n\n0.4 \n\nH2;c  _'_~4W. ;11 \n\n- I \n\n+ \n\nH3  ~ \u2022 ...,p.~~  Rep  ~ \nL1  -..,~. v..  ..At '~\"lf\"'o ~ \n+ \n- +~~\"4 = e  . . . . .  ~ \n+ \n\nL2 \n\n+ \n\nL4 \n\n+ \n\nL3  ::\"I-\u00b7~~ ~ \n-1$ f- ...... \u00b7 A.E:::::;?  <:::!>  <P ~ \n81  ~'f'r4'i\"'Qf4;.~TIN'I\"m\"'''''~''i \n+ \n;,\"1Y\u00a5\".-U'lt ~'tt~'.'~'~'~\"'fH','t1 \n82 \n+ \nU1  ;'~t.,,=,,,~~FW\"\" ~ .. _~ \n\n+ \n\n+ \n\nU2  ~ I-- iiIIe<>\"\"  ,;I6'O'~'  t'4ac*'\" , \nU3  -.... ro1~C--_ 'k .   \u2022  ...  -\nUS  :+~[P'~Q\"\"'~ \"' ..... ~ .. _ \n\nU4  ~~ 111(ok i.  tdt .. 'IWoio'\" \n\n\"M I~ C \n\n+ \n\n+ \n\n- Detected targets \n\n- Undetected targets \n\nFigure  2:  Left  panel:  Event-related  potentials  (ERPs)  in  response  to  undetected \n(bold  traces)  and  detected  (faint  traces)  noise  targets during two half-hour sessions. \nRight  panel:  Same ERP signals filtered  using an leA weight  matrix trained on the \nERP data. \n\n\fIndependent Component Analysis  of Electroencephalographic  Data \n\n151 \n\ncomponents of the (larger)  undetected  target response.  We  suggest  these  represent \nthe time course  of the locus  (either focal  or distributed)  of brain response  activity, \nand  may represent  a  solution  to  the  longstanding  problem of objectively  dividing \nevoked  responses  into  neurobiologically  meaningful,  temporally  overlapping  sub(cid:173)\ncomponents. \n\n4  Conclusions \n\nICA appears to be a promising new analysis tool for human EEG and ERP research. \nIt can isolate a wide range of artifacts to a few  output channels while removing them \nfrom  remaining channels.  These  may in  turn  represent  the time course  of activity \nin longlasting or transient independent  'brain sources' on which  the algorithm con(cid:173)\nverges  reliably.  By  incorporating  higher-order  statistical  information,  ICA  avoids \nthe  non-uniqueness  associated  with  decorrelating  decompositions.  The  algorithm \nalso appears  to  be  useful  for  decomposing evoked  response  data into spatially dis(cid:173)\ntinct subcomponents,  while  measures of nonstationarity in  the ICA source  solution \nmay be useful  for  observing brain state changes. \n\nAcknowledgments \n\nThis report was supported in part by a grant (ONR.Reimb .30020.6429) to the Naval \nHealth  Research  Center  by  the  Office  of Naval  Research.  The  views  expressed  in \nthis article are those of the  authors and do not reflect  the official policy or position \nof the  Department of the  Navy,  Department of Defense,  or  the  U.S.  Government. \nDr.  Bell  is supported  by  grants from the Office  of Naval Research  and  the  Howard \nHughes  Medical  Institute. \n\nReferences \n\n[1]  A.J.  Bell  &  T.J. Sejnowski  (1995).  An information-maximization approach  to \n\nblind separation and  blind deconvolution,  Neural  Computation 7:1129-1159 . \n[2]  A.J.  Bell  &  T.J.  Sejnowski  (1995).  Fast  blind  separation  based  on  informa(cid:173)\n\ntion  theory,  in  Proc.  Intern.  Symp.  on  Nonlinear  Theory  and  Applications \n(NOLTA),  Las Vegas,  Dec.  1995. \n\n[3]  P.  Comon  (1994)  Independent  component  analysis,  a  new  concept?  Signal \n\nprocessing 36:287-314. \n\n[4]  A.M.  Dale  &  M.1.  Sereno  (1993)  EEG  and  MEG  source  localization:  a  linear \n\napproach.  J.  Cogn.  Neurosci.  5:162. \n\n[5]  R.  Galambos  &  S.  Makeig.  (1989)  Dynamic  changes  in  steady-state  poten(cid:173)\n\ntials.  In  Erol  Basar  (ed.),  Dynamics  of Sensory  and  Cognitive  Processing  of \nthe  Brain,  102-122. Berlin:Springer-Verlag. \n\n[6]  S.  Makeig  &  R.  Galambos.  (1989)  The  CERP:  Event-related  perturbations \nin  steady-state  responses.  In  E.  Basar &  T.H.  Bullock  (ed.),  Brain  Dynamics: \nProgress  and  Perspectives,  375-400.  Berlin:Springer-Verlag. \n\n[7]  T-P. Jung,  S.  Makeig,  M.  Stensmo, &  T. Sejnowski.  Estimating alertness  from \n\nthe  EEG  power  spectrum.  Submitted for  publication. \n\n[8]  S.  Makeig  &  M.  Inlow  (1993)  Lapses  in  alertness:  Coherence  of fluctuations \nin  performance  and  EEG  spectrum.  Electroencephalog.  din.  N europhysiolog. \n86:23-35. \n\n\f", "award": [], "sourceid": 1091, "authors": [{"given_name": "Scott", "family_name": "Makeig", "institution": null}, {"given_name": "Anthony", "family_name": "Bell", "institution": null}, {"given_name": "Tzyy-Ping", "family_name": "Jung", "institution": null}, {"given_name": "Terrence", "family_name": "Sejnowski", "institution": null}]}