Purpose: To determine the differences in functional connectivity among brain regions during the different stages of the human sleep cycle

Duan, Grace, \u2715

Malhotra, Sameeksha, \u2715

Parrish, Todd B

English

Illinois Mathematics and Science Academy: DigitalCommons@IMSA

Are	  there	  differences	  in	  active	  brain	  regions	  during	  each	  of	  the	  3ive	  sleep	  stages?	  If	  so,	  what	  are	  they?	  ACTIVE	  BRAIN	  REGIONS	  DURING	  SLEEP	  USING	  ELECTROENCEPHALOGRAPHY-­‐FUNCTIONAL	  MAGNETIC	  RESONANCE	  IMAGING	  Grace	  Duan	  &	  Sameeksha	  Malhotra	  Illinois	  Mathematics	  and	  Science	  Academy	   Todd	  Parrish	  Northwestern	  University	  Feinberg	  School	  of	  Medicine	  FOCUSING	  QUESTION	  ABSTRACT	  INTRODUCTION	   ACKNOWLEDGEMENTS	  METHODS	  1.  Obtain	  consent	  from	  typical	  adult	  volunteers	  aged	  18	  to	  60.	  2.  Position	  the	  Neuroscan	  Maglink	  electroencephalogram	  (EEG)	  on	  the	  scalp	  of	  the	  volunteer.	  3.  Relocate	  the	  subject	  into	  the	  magnetic	  resonance	  room	  and	  carefully	  position	  the	  subject	  lying	  down	  in	  the	  scanner.	  	  4.  Once	  the	  subject’s	  head	  is	  properly	  placed	  in	  the	  head	  coil,	  they	  are	  asked	  to	  go	  try	  to	  sleep..	  The	  subject	  should	  only	  remain	  in	  the	  scanner	  for	  up	  to	  90	  minutes.	  	  5.  This	  is	  to	  be	  repeated	  with	  each	  volunteer.	  6.  Data	  from	  the	  EEG	  was	  collected	  with	  the	  Neuroscan	  ACQUIRE	  software	  and	  the	  fMRI	  was	  collected	  simultaneously	  with	  Oxford	  University’s	  Functional	  Software	  Library	  (FSL)	  software.	  	  7.  Identify	  and	  record	  the	  sleep	  stages	  based	  on	  the	  EEG	  wave	  characteristics	  in	  8	  second	  intervals.	  8.  Determine	  which	  time	  intervals	  of	  the	  EEG	  data	  match	  with	  which	  images	  generated	  by	  fMRI.	  9.  Separate	  the	  image	  slides	  into	  their	  respective	  folders	  for	  each	  sleep	  stage.	  10. Running	  a	  pipeline	  in	  NUNDA,	  calculate	  the	  functional	  connectivity	  values	  for	  the	  regions	  of	  interest	  for	  each	  sleep	  stage.	  11. Using	  Mango	  software,	  visualize	  the	  brain	  in	  each	  sleep	  stage	  and	  the	  functional	  connectivity	  regions	  that	  are	  colored.	  12. Using	  Matlab	  to	  create	  correlation	  matrices	  for	  each	  sleep	  stage	  which	  show	  the	  connectivity	  of	  the	  ROIs	  quantitatively.	  CONCLUSION	  •  Previous	  results	  concluded	  that	  activity	  in	  ROIs	  in	  REM	  sleep	  is	  widespread	  over	  various	  regions	  of	  the	  brain,	  while	  activity	  in	  ROIS	  in	  sleep	  stage	  two	  is	  centralized	  to	  the	  region	  of	  interest.	  •  These	  results	  are	  consistent	  with	  previous	  results.	  •  Less	  functional	  connectivity	  in	  stages	  one	  and	  two.	  •  More	  inter-­‐region	  activity	  in	  REM	  sleep.	  •  ROIs	  in	  wakefulness	  and	  REM	  sleep	  also	  depict	  neuronal	  activity	  throughout	  the	  entire	  brain.	  •  Wakefulness	  shows	  a	  larger	  amount	  of	  widespread	  neuronal	  activity	  than	  REM.	  •  ROIs	  in	  sleep	  stages	  one,	  two,	  and	  three	  are	  all	  localized	  upon	  the	  region	  of	  interest.	  •  There	  is	  little	  discrepancy	  between	  these	  stages.	  •  In	  subject	  two,	  wakefulness,	  sleep	  stage	  one,	  and	  stage	  three	  all	  show	  activity	  throughout	  the	  entire	  brain,	  leading	  us	  to	  believe	  that	  only	  in	  sleep	  stage	  two	  is	  the	  neuronal	  activity	  truly	  focused	  to	  the	  region	  of	  interest.	  •  Correlation	  matrices	  show	  the	  amount	  of	  correlation	  between	  the	  various	  regions	  of	  the	  brain	  by	  showing	  either	  negative,	  none,	  or	  positive	  correlation.	  •  Limitations	  include	  the	  fact	  that	  quality	  of	  sleep	  is	  uncertain	  •  45	  minute	  session	  in	  the	  middle	  of	  the	  day	  •  Duration	  of	  each	  sleep	  stage	  varied	  as	  there	  were	  different	  number	  of	  volumes	  •  Few	  good	  subjects	  –	  dif3icult	  to	  sleep	  in	  MRI	  •  Future	  work	  includes	  testing	  abnormal	  subjects,	  as	  well	  as	  creating	  a	  template	  network	  for	  normal	  subjects	  for	  each	  sleep	  stage.	  •  May	  help	  in	  diagnosing	  sleep	  disorders	  by	  comparing	  the	  disorders	  to	  the	  template.	  RESULTS	  Figure	  2.	  Activity	  detected	  by	  the	  functional	  magnetic	  resonance	  imaging	  (fMRI)	  at	  the	  left	  hippocampal	  electrode	  for	  subject	  one.	  These	  images	  show	  activity	  associated	  with	  the	  left	  hippocampus	  during	  wakefulness	  (d),	  sleep	  stage	  one	  (e),	  stage	  two	  (f),	  stage	  three	  (g)	  and	  REM	  sleep	  (h).	  These	  display	  the	  subject’s	  brain	  from	  the	  superior	  (top),	  posterior	  (bottom	  left),	  and	  lateral	  (bottom	  right)	  views.	  	  	  Figure	  3.	  Activity	  detected	  by	  the	  functional	  magnetic	  resonance	  imaging	  (fMRI)	  at	  the	  left	  posterior	  cingulate	  electrode	  for	  subject	  two	  These	  images	  show	  activity	  associated	  with	  the	  left	  posterior	  cingulate	  during	  wakefulness	  (i),	  sleep	  stage	  one	  (j),	  stage	  two	  (k),	  stage	  three	  (l)	  and	  REM	  sleep	  (m).	  These	  display	  the	  subject’s	  brain	  from	  the	  superior	  (top),	  posterior	  (bottom	  left),	  and	  lateral	  (bottom	  right)	  views.	  (a)	   (b)	   (c)	  (g)	  (f)	  (e)	  (d)	  (j)	  (i)	  (h)	  REFERENCES	  	  With	  techniques	  allowing	  the	  simultaneous	  acquisition	  of	  electroencephalogram	  (EEG)	  and	  functional	  magnetic	  resonance	  imaging	  (fMRI)	  data,	  active	  brain	  regions	  during	  different	  stages	  of	  the	  human	  sleep	  cycle	  were	  determined.	  Data	  were	  collected	  using	  a	  Siemens	  3T	  Trio	  magnet	  with	  standard	  BOLD	  sequence	  acquired	  for	  45	  minutes	  while	  the	  subject	  slept	  and	  Neuroscan	  Maglink	  MRI-­‐compatible	  EEG.	  The	  EEG	  data	  oscillations	  were	  used	  to	  segment	  the	  sleep	  into	  the	  3ive	  sleep	  stages.	  The	  respective	  MR	  images	  were	  grouped,	  motion	  corrected,	  and	  spatially	  smoothed.	  Regions	  of	  interest	  (ROIs)	  were	  extracted	  to	  create	  correlation	  maps,	  visualized	  using	  Mango	  software.	  Correlation	  matrices	  were	  created	  using	  MATLAB	  displaying	  neuronal	  connectivity	  among	  ROIs.	  Results	  suggest	  that	  ROI	  brain	  activity	  is	  localized	  during	  sleep	  stage	  two.	  In	  rapid	  eye	  movement	  (REM)	  sleep,	  ROI	  brain	  activity	  is	  also	  present	  in	  most	  other	  brain	  regions.	  Hippocampal	  activity	  is	  most	  prevalent	  in	  all	  investigated	  stages,	  followed	  by	  thalamus,	  posterior	  cingulate,	  and	  amygdala	  activity.	  Brain	  activity	  in	  stage	  one	  and	  REM	  is	  similar,	  although	  REM	  activity	  is	  less	  concentrated	  to	  the	  ROI.	  The	  correlation	  matrix	  results	  are	  consistent	  with	  the	  qualitative	  analysis.	  EEG-­‐fMRI	  data	  can	  lead	  to	  an	  improved	  understanding	  of	  brain	  activity	  during	  sleep,	  which	  may	  help	  in	  diagnosing	  sleep	  disorders.	  •  Human	  sleep	  cycle	  is	  divided	  into	  rapid	  eye	  movement	  (REM)	  and	  non-­‐rapid	  eye	  movement	  (NREM)	  stages,	  all	  3ive	  of	  which	  have	  distinct	  EEG	  wave	  characteristics	  like	  frequency	  and	  amplitude	  (Oropesa,	  Cycon,	  &	  Jobert	  1999)	  •  Stage	  1	  –	  low-­‐voltage	  with	  distinct	  alpha	  (8-­‐13	  Hz)	  and	  theta	  (4-­‐8	  Hz)	  activity	  with	  occasional	  vertex	  spikes	  •  Stage	  2	  –	  sleep	  spindles	  and	  K-­‐complexes;	  high	  voltage	  delta	  waves	  (0-­‐4	  Hz)	  •  Stages	  3	  and	  4	  –	  deep	  sleep	  with	  delta	  waves	  •  REM	  –	  dreaming	  occurs;	  low	  amplitude	  patterns	  similar	  to	  stage	  1	  (Ebrahimi	  et	  al.	  2008).	  •  Many	  sleep	  studies	  on	  role	  of	  brain	  regions	  during	  sleep	  •  Thalamus	  –	  regulating	  sleep-­‐wake	  cycle	  and	  circadian	  rhythms	  (Tinuper	  et	  al.	  1989)	  •  Posterior	  cingulate	  cortex	  –	  most	  active	  during	  internally-­‐directed	  activity	  (Leech,	  Braga,	  &	  Sharp	  2012)	  •  Amygdala	  –	  processing	  emotion	  and	  sleep	  regulation	  (Benca	  et	  al.	  2000)	  •  Hippocampus	  –	  consolidates	  memories	  (Tulving	  &	  Markowitsch	  1998)	  •  Sleep	  disorders	  like	  obstructive	  sleep	  apnea	  (OSA)	  cause	  neural	  disruption	  and	  health	  consequences	  (Pascual	  et	  al.	  2001)	  	  We	  would	  like	  to	  thank	  Dr.	  Todd	  Parrish,	  the	  head	  of	  the	  Parrish	  Neuroimaging	  Laboratory	  at	  Feinberg	  School	  of	  Medicine	  at	  Northwestern	  University,	  for	  serving	  as	  our	  advisor	  for	  two	  years	  throughout	  this	  investigation.	  His	  commitment,	  patience,	  and	  encouragement	  were	  crucial	  to	  this	  project.	  	  We	  would	  also	  like	  to	  acknowledge	  Dr.	  Scheppler	  and	  the	  Student	  Inquiry	  and	  Research	  staff	  of	  the	  Illinois	  Mathematics	  and	  Science	  Academy	  for	  providing	  us	  the	  opportunity	  to	  pursue	  this	  research	  project,	  giving	  us	  a	  plethora	  of	  resources	  from	  which	  to	  draw	  scienti3ic	  knowledge,	  and	  guiding	  us	  through	  the	  process	  of	  scienti3ic	  inquiry	  every	  step	  of	  the	  way.	  •  Benca,	  R.,	  Obermeyer,	  W.,	  Shelton,	  S.,	  Droster,	  J.,	  &	  Kalin,	  N.	  (2000).	  Effects	  of	  amygdala	  lesions	  on	  sleep	  in	  rhesus	  monkeys.	  Brain	  Research.	  Retrieved	  from	  http://www.researchgate.net/publication/12312703_Effects_of_amygdala_lesions_on_sleep_in_rhesus_monkeys.	  •  Ebrahimi,	  F.,	  Mikaeili,	  M.,	  Estrada,	  E.,	  &	  Nazeran,	  H.	  (2008).	  Automatic	  sleep	  stage	  classi3ication	  based	  on	  EEG	  signals	  by	  using	  neural	  networks	  and	  wavelet	  packet	  coef3icients.	  Conference	  Proceedings	  of	  the	  IEEE	  Engineering	  in	  Medicine	  and	  Biology	  Society,	  1151-­‐1154.	  doi:	  10.1109/IEMBS.2008.4649365.	  •  Leech,	  R.,	  Braga,	  R.,	  &	  Sharp,	  D.	  (2012).	  Echoes	  of	  the	  brain	  within	  the	  posterior	  cingulate	  cortex.	  The	  Journal	  of	  Neuroscience,	  32(1),	  215-­‐222.	  doi:	  10.1523/JNEUROSCI.3689-­‐11-­‐2012.	  •  Oropesa,	  E.,	  Cycon,	  H.	  L.,	  Jobert,	  M.	  (1999).	  Sleep	  stage	  classi3ication	  using	  wavelet	  transform	  and	  neural	  network.	  International	  Computer	  Science	  Institute.	  Retrieved	  from	  http://www.ics.uci.edu/~dgorur/papers/01007762.pdf.	  •  Salin-­‐Pascual,	  R.,	  Gerashchenko,	  D.,	  Greco,	  M.,	  Blanco-­‐Centurion,	  C.,	  &	  Shiromani,	  P.	  (2001).	  Hypothalamic	  regulation	  of	  sleep.	  Neuropsychopharmacology,	  25(55),	  21-­‐27.	  http://www.researchgate.net/publication/11671242_Hypothalamic_regulation_of_sleep/links/0deec520b9b98e9f06000000.	  •  Tinuper,	  P.,	  Montagna,	  P.,	  Medori,	  R.,	  Cortelli,	  P.,	  Zucconi,	  M.,	  Baruzzi,	  A.,	  &	  Lugaresi,	  E.	  (1989).	  The	  thalamus	  participates	  in	  the	  regulation	  of	  the	  sleep-­‐wake	  cycle.	  A	  clinic-­‐pathological	  study	  in	  fatal	  familial	  thalamic	  degeneration.	  Electroencephalography	  and	  Clinical	  Neurophysiology,	  73(2),	  117-­‐123.	  doi:	  10.1016/0013-­‐4694(89)90190-­‐9.	  •  Tulving,	  E.	  &	  Markowitsch,	  H.	  (1998).	  Episodic	  and	  declarative	  memory:	  role	  of	  the	  hippocampus.	  Hippocampus,	  8(3),	  198-­‐204.	  doi:	  10.1002/(SICI)1098-­‐1063(1998)8:3<198::AID-­‐HIPO2>3.0.CO;2-­‐G.	  Figure	  1.	  Previous	  results	  show	  activity	  detected	  by	  the	  functional	  magnetic	  resonance	  imaging	  (fMRI)	  at	  the	  left	  hippocampal	  and	  left	  posterior	  cingulate	  electrode	  for	  subject	  one.	  These	  images	  show	  activity	  associated	  with	  the	  left	  hippocampus	  and	  left	  posterior	  cingulate	  during	  sleep	  stage	  one	  (a),	  stage	  two	  (b),	  and	  REM	  sleep	  (c).	  These	  display	  the	  subject’s	  brain	  from	  the	  superior	  (top),	  posterior	  (bottom	  left),	  and	  lateral	  (bottom	  right)	  views.	  	  	  Hippocampus	   Posterior	  Cingulate	  Cortex	  (a)	   (b)	   (c)	   (a)	   (b)	   (c)	  (d)	   (e)	   (f)	   (g)	   (h)	  (i)	   (j)	   (k)	   (l)	   (m)	  

Active Brain Regions During Sleep Using Electroencephalography-Functional Magnetic Resonance Imaging

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Active Brain Regions During Sleep Using Electroencephalography-Functional Magnetic Resonance Imaging

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