SHORT COMMUNICATION Frontal theta activity in humans increases with memory load in a working memory task

Recent theoretical work has suggested that brain oscillations in the theta band are involved in active maintenance and recall of working memory representations. To test this theoretical framework we recorded neuromagnetic responses from 10 subjects performing the Sternberg task. Subjects were required to retain a list of 1, 3, 5 or 7 visually presented digits during a 3-s retention period. During the retention period we observed ongoing frontal theta activity in the 7‐8.5-Hz band recorded by sensors over frontal brain areas. The activity in the theta band increased parametrically with the number of items retained in working memory. A time‐frequency analysis revealed that the task-dependent theta was present during the retention period and during memory scanning. Following the memory task the theta activity was reduced. These results suggest that theta oscillations generated in frontal brain regions play an active role in memory maintenance.

[1]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[2]  M. Tanaka,et al.  Periodic appearance of theta rhythm in the frontal midline area during performance of a mental task. , 1980, Electroencephalography and clinical neurophysiology.

[3]  H. Asada,et al.  Frontal midline theta rhythms reflect alternative activation of prefrontal cortex and anterior cingulate cortex in humans , 1999, Neuroscience Letters.

[4]  S. Roux,et al.  Auditory stimulus intensity responses and frontal midline theta rhythm. , 1993, Electroencephalography and clinical neurophysiology.

[5]  M A B BRAZIER,et al.  Cross-correlation and autocorrelation studies of electroencephalographic potentials. , 1952, Electroencephalography and clinical neurophysiology.

[6]  L. Parkkonen,et al.  122-channel squid instrument for investigating the magnetic signals from the human brain , 1993 .

[7]  T. Inouye,et al.  Medial prefrontal cortex generates frontal midline theta rhythm. , 1999, Neuroreport.

[8]  A. Burgess,et al.  Short duration synchronization of human theta rhythm during recognition memory , 1997, Neuroreport.

[9]  Oswaldo Baffa,et al.  Theta Oscillations and Human Navigation: A Magnetoencephalography Study , 2002, Journal of Cognitive Neuroscience.

[10]  Daphne N. Yu,et al.  High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. , 1997, Cerebral cortex.

[11]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[12]  N. Takahashi,et al.  Frontal Midline Theta Rhythm in Young Healthy Adults , 1997, Clinical EEG.

[13]  Adrian M. Owen,et al.  The role of the lateral frontal cortex in mnemonic processing: the contribution of functional neuroimaging , 2000, Experimental Brain Research.

[14]  Joseph R. Madsen,et al.  Human theta oscillations exhibit task dependence during virtual maze navigation , 1999, Nature.

[15]  Kazuhiro Shinosaki,et al.  Potential flow of frontal midline theta activity during a mental task in the human electroencephalogram , 1994, Neuroscience Letters.

[16]  Wolfgang Klimesch,et al.  The Functional Significance of Absolute Power with Respect to Event-Related Desynchronization , 2004, Brain Topography.

[17]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[18]  R. Näätänen,et al.  Gabor filters: an informative way for analysing event-related brain activity , 1995, Journal of Neuroscience Methods.

[19]  K. Inanaga,et al.  Frontal midline theta rhythm and mental activity , 1998, Psychiatry and Clinical Neurosciences.

[20]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  O Jensen,et al.  An Oscillatory Short-Term Memory Buffer Model Can Account for Data on the Sternberg Task , 1998, The Journal of Neuroscience.

[22]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[23]  J. Lisman,et al.  Physiologically realistic formation of autoassociative memory in networks with theta/gamma oscillations: role of fast NMDA channels. , 1996, Learning & memory.

[24]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[25]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Sternberg.  High-Speed Scanning in Human Memory , 1966, Science.

[27]  J E Lisman,et al.  Storage of 7 +/- 2 short-term memories in oscillatory subcycles , 1995, Science.

[28]  Arne D. Ekstrom,et al.  NMDA Receptor Antagonism Blocks Experience-Dependent Expansion of Hippocampal “Place Fields” , 2001, Neuron.

[29]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[30]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

[31]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

[32]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[33]  O. Jensen,et al.  A New Method to Identify Multiple Sources of Oscillatory Activity from Magnetoencephalographic Data , 2002, NeuroImage.