Cortical Spatio-temporal Dynamics Underlying Phonological Target Detection in Humans

Selective processing of task-relevant stimuli is critical for goal-directed behavior. We used electrocorticography to assess the spatio-temporal dynamics of cortical activation during a simple phonological target detection task, in which subjects press a button when a prespecified target syllable sound is heard. Simultaneous surface potential recordings during this task revealed a highly ordered temporal progression of high gamma (HG, 70–200 Hz) activity across the lateral hemisphere in less than 1 sec. The sequence demonstrated concurrent regional sensory processing of speech syllables in the posterior superior temporal gyrus (STG) and speech motor cortex, and then transitioned to sequential task-dependent processing from prefrontal cortex (PFC), to the final motor response in the hand sensorimotor cortex. STG activation was modestly enhanced for target over nontarget sounds, supporting a selective gain mechanism in early sensory processing, whereas PFC was entirely selective to targets, supporting its role in guiding response behavior. These results reveal that target detection is not a single cognitive event, but rather a process of progressive target selectivity that involves large-scale rapid parallel and serial processing in sensory, cognitive, and motor structures to support goal-directed human behavior.

[1]  J. Rauschecker,et al.  Phoneme and word recognition in the auditory ventral stream , 2012, Proceedings of the National Academy of Sciences.

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

[3]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[4]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[5]  Ernst Niebur,et al.  Effect of Stimulus Intensity on the Spike–Local Field Potential Relationship in the Secondary Somatosensory Cortex , 2008, The Journal of Neuroscience.

[6]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[7]  Diana L Miglioretti,et al.  Cortical Sites Critical for Speech Discrimination in Normal and Impaired Listeners , 2005, The Journal of Neuroscience.

[8]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[9]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[10]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[11]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[12]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

[13]  M. Goldstein,et al.  Neuroperceptual Differences in Consonant and Vowel Discrimination: As Revealed by Direct Cortical Electrical Interference , 1997, Cortex.

[14]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[15]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[16]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. , 1995, Electroencephalography and clinical neurophysiology.

[17]  S. Hillyard,et al.  Electrical Signs of Selective Attention in the Human Brain , 1973, Science.

[18]  G. Schalk,et al.  Brain-Computer Interfaces Using Electrocorticographic Signals , 2011, IEEE Reviews in Biomedical Engineering.

[19]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[20]  Mitchell Steinschneider,et al.  Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. , 2008, Cerebral cortex.

[21]  Edward F Chang,et al.  Real-time, time–frequency mapping of event-related cortical activation , 2012, Journal of neural engineering.

[22]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[23]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[24]  D H HUBEL,et al.  "Attention" Units in the Auditory Cortex , 1959, Science.

[25]  Mark D'Esposito,et al.  From cognitive to neural models of working memory , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[27]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[28]  Rajesh P. N. Rao,et al.  Real-time functional brain mapping using electrocorticography , 2007, NeuroImage.

[29]  R. Romo,et al.  Neuronal correlates of subjective sensory experience , 2005, Nature Neuroscience.

[30]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[31]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[32]  M. Berger,et al.  High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. , 2005, Journal of neurophysiology.

[33]  C. Crainiceanu,et al.  Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. , 2005, Brain : a journal of neurology.

[34]  Erik Edwards,et al.  Comparison of time-frequency responses and the event-related potential to auditory speech stimuli in human cortex. , 2009, Journal of neurophysiology.

[35]  Ciprian M. Crainiceanu,et al.  Dynamics of large-scale cortical interactions at high gamma frequencies during word production: Event related causality (ERC) analysis of human electrocorticography (ECoG) , 2011, NeuroImage.

[36]  Robert T. Knight,et al.  Localization of neurosurgically implanted electrodes via photograph–MRI–radiograph coregistration , 2008, Journal of Neuroscience Methods.

[37]  E. Miller,et al.  All My Circuits: Using Multiple Electrodes to Understand Functioning Neural Networks , 2008, Neuron.

[38]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception. Brazier Award-winning article, 2001. , 2001, Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology.

[39]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[40]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[41]  N. Barbaro,et al.  Spatiotemporal Dynamics of Word Processing in the Human Brain , 2007, Front. Neurosci..

[42]  Mark D'Esposito,et al.  Searching for “the Top” in Top-Down Control , 2005, Neuron.

[43]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[44]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[45]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[46]  Brian E. Russ,et al.  Prefrontal Neurons Predict Choices during an Auditory Same-Different Task , 2008, Current Biology.