Robust discrimination between EEG responses to categories of environmental sounds in early coma

Humans can recognize categories of environmental sounds, including vocalizations produced by humans and animals and the sounds of man-made objects. Most neuroimaging investigations of environmental sound discrimination have studied subjects while consciously perceiving and often explicitly recognizing the stimuli. Consequently, it remains unclear to what extent auditory object processing occurs independently of task demands and consciousness. Studies in animal models have shown that environmental sound discrimination at a neural level persists even in anesthetized preparations, whereas data from anesthetized humans has thus far provided null results. Here, we studied comatose patients as a model of environmental sound discrimination capacities during unconsciousness. We included 19 comatose patients treated with therapeutic hypothermia (TH) during the first 2 days of coma, while recording nineteen-channel electroencephalography (EEG). At the level of each individual patient, we applied a decoding algorithm to quantify the differential EEG responses to human vs. animal vocalizations as well as to sounds of living vocalizations vs. man-made objects. Discrimination between vocalization types was accurate in 11 patients and discrimination between sounds from living and man-made sources in 10 patients. At the group level, the results were significant only for the comparison between vocalization types. These results lay the groundwork for disentangling truly preferential activations in response to auditory categories, and the contribution of awareness to auditory category discrimination.

[1]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[2]  M. Kiefer,et al.  Attentional sensitization of unconscious cognition: task sets modulate subsequent masked semantic priming. , 2010, Journal of experimental psychology. General.

[3]  P. Sajda,et al.  Temporal characterization of the neural correlates of perceptual decision making in the human brain. , 2006, Cerebral cortex.

[4]  Bruno L. Giordano,et al.  Abstract encoding of auditory objects in cortical activity patterns. , 2013, Cerebral cortex.

[5]  Karen Smith,et al.  Treatment of Comatose Survivors of Out-of-hospital Cardiac Arrest With Induced Hypothermia , 2003 .

[6]  Christoph M. Michel,et al.  Decoding stimulus-related information from single-trial EEG responses based on voltage topographies , 2012, Pattern Recognit..

[7]  Norma Wioland,et al.  Cortical Information Processing in Coma , 2009, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[8]  M. Kiefer Executive control over unconscious cognition: attentional sensitization of unconscious information processing , 2012, Front. Hum. Neurosci..

[9]  M. Murray,et al.  A Tutorial Review of Electrical Neuroimaging From Group-Average to Single-Trial Event-Related Potentials , 2012, Developmental neuropsychology.

[10]  Pascal Belin,et al.  Electrophysiological evidence for an early processing of human voices , 2009, BMC Neuroscience.

[11]  Micah M. Murray,et al.  The role of actions in auditory object discrimination , 2009, NeuroImage.

[12]  Shlomo Bentin,et al.  Neural sensitivity to human voices: ERP evidence of task and attentional influences. , 2003, Psychophysiology.

[13]  S. R. Butler,et al.  Electrophysiological indicator of awakening from coma , 1993, The Lancet.

[14]  Yale E Cohen,et al.  Coding of auditory-stimulus identity in the auditory non-spatial processing stream. , 2008, Journal of neurophysiology.

[15]  E. DeYoe,et al.  Distinct Cortical Pathways for Processing Tool versus Animal Sounds , 2005, The Journal of Neuroscience.

[16]  A. Kramer,et al.  Comparison of the Full Outline of UnResponsiveness Score and the Glasgow Coma Scale in Predicting Mortality in Critically Ill Patients* , 2015, Critical care medicine.

[17]  Mauro Oddo,et al.  Prognostication after cardiac arrest and hypothermia: A prospective study , 2010, Annals of neurology.

[18]  Joachim Gross,et al.  The early spatio-temporal correlates and task independence of cerebral voice processing studied with MEG. , 2013, Cerebral cortex.

[19]  Xiaofeng Jia,et al.  Hypothermia Amplifies Somatosensory-evoked Potentials in Uninjured Rats , 2012, Journal of neurosurgical anesthesiology.

[20]  Rainer Goebel,et al.  "Who" Is Saying "What"? Brain-Based Decoding of Human Voice and Speech , 2008, Science.

[21]  Stephanie Clarke,et al.  A Temporal Hierarchy for Conspecific Vocalization Discrimination in Humans , 2010, The Journal of Neuroscience.

[22]  Dominique Morlet,et al.  Novelty P3 elicited by the subject’s own name in comatose patients , 2008, Clinical Neurophysiology.

[23]  Maarten De Vos,et al.  Let's face it, from trial to trial: Comparing procedures for N170 single-trial estimation , 2012, NeuroImage.

[24]  G. Recanzone,et al.  Representation of Con-Specific Vocalizations in the Core and Belt Areas of the Auditory Cortex in the Alert Macaque Monkey , 2008, The Journal of Neuroscience.

[25]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[26]  J. Rauschecker,et al.  Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category , 2010, The Journal of Neuroscience.

[27]  Pascal Belin,et al.  Is voice processing species-specific in human auditory cortex? An fMRI study , 2004, NeuroImage.

[28]  Yale E Cohen,et al.  Acoustic features of rhesus vocalizations and their representation in the ventrolateral prefrontal cortex. , 2007, Journal of neurophysiology.

[29]  R. Auer,et al.  Hypoxia, hyperoxia, ischemia, and brain necrosis , 2000, Neurology.

[30]  Robyn L McClelland,et al.  Validation of a new coma scale: The FOUR score , 2005, Annals of neurology.

[31]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[32]  M. Mishkin,et al.  Species-specific calls evoke asymmetric activity in the monkey's temporal poles , 2004, Nature.

[33]  Srivas Chennu,et al.  Arousal Modulates Auditory Attention and Awareness: Insights from Sleep, Sedation, and Disorders of Consciousness , 2011, Front. Psychology.

[34]  Pascal Belin,et al.  Right temporal TMS impairs voice detection , 2011, Current Biology.

[35]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

[36]  M. Schaller,et al.  Pathogenetic and prognostic significance of altered coagulation and fibrinolysis in acute lung injury/acute respiratory distress syndrome , 2006 .

[37]  Xiaoqin Wang,et al.  Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. , 2001, Journal of neurophysiology.

[38]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[39]  Noël Staeren,et al.  Sound Categories Are Represented as Distributed Patterns in the Human Auditory Cortex , 2009, Current Biology.

[40]  N. Logothetis,et al.  A voice region in the monkey brain , 2008, Nature Neuroscience.

[41]  J. Guérit,et al.  ERPs obtained with the auditory oddball paradigm in coma and altered states of consciousness: clinical relationships, prognostic value, and origin of components , 1999, Clinical Neurophysiology.

[42]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Dominique Morlet,et al.  Predictive value of sensory and cognitive evoked potentials for awakening from coma , 2004, Neurology.

[44]  Stephanie Clarke,et al.  Perceptual and semantic contributions to repetition priming of environmental sounds. , 2010, Cerebral cortex.

[45]  Paula Breen,et al.  WHO IS TO SAY , 1967 .

[46]  R. Zatorre,et al.  Cortical Processing of Complex Auditory Stimuli during Alterations of Consciousness with the General Anesthetic Propofol , 2006, Anesthesiology.

[47]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[48]  Lucas Spierer,et al.  Auditory perceptual decision-making based on semantic categorization of environmental sounds , 2012, NeuroImage.

[49]  Steven Laureys,et al.  Comparison of the Full Outline of UnResponsiveness and Glasgow Liege Scale/Glasgow Coma Scale in an Intensive Care Unit Population , 2011, Neurocritical care.

[50]  B. de Gelder,et al.  Mismatch negativity predicts recovery from the vegetative state , 2007, Clinical Neurophysiology.

[51]  Jean-Philippe Thiran,et al.  What and Where in human audition: selective deficits following focal hemispheric lesions , 2002, Experimental Brain Research.

[52]  Anne-Lise Giraud,et al.  Distinct functional substrates along the right superior temporal sulcus for the processing of voices , 2004, NeuroImage.

[53]  Markus Kiefer,et al.  Masked Priming of Conceptual Features Reveals Differential Brain Activation during Unconscious Access to Conceptual Action and Sound Information , 2013, PloS one.

[54]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[55]  Christoph Kayser,et al.  Voice Cells in the Primate Temporal Lobe , 2011, Current Biology.

[56]  Micah M. Murray,et al.  Rapid Brain Discrimination of Sounds of Objects , 2006, The Journal of Neuroscience.

[57]  M. Murray,et al.  Automated Auditory Mismatch Negativity Paradigm Improves Coma Prognostic Accuracy After Cardiac Arrest and Therapeutic Hypothermia , 2014, Journal of clinical neurophysiology.

[58]  Thomas Koenig,et al.  A Method to Determine the Presence of Averaged Event-Related Fields Using Randomization Tests , 2010, Brain Topography.

[59]  Natalie M. Trumpp,et al.  Losing the sound of concepts: Damage to auditory association cortex impairs the processing of sound-related concepts , 2013, Cortex.

[60]  Lucas Spierer,et al.  Progression of auditory discrimination based on neural decoding predicts awakening from coma. , 2013, Brain : a journal of neurology.

[61]  D Morlet,et al.  Mismatch negativity and late auditory evoked potentials in comatose patients , 1999, Clinical Neurophysiology.

[62]  Markus Kiefer,et al.  Neuroplasticity of semantic representations for musical instruments in professional musicians , 2011, NeuroImage.

[63]  Lars Hausfeld,et al.  Pattern analysis of EEG responses to speech and voice: Influence of feature grouping , 2012, NeuroImage.

[64]  Steven Laureys,et al.  Mismatch negativity to the patient’s own name in chronic disorders of consciousness , 2008, Neuroscience Letters.

[65]  N. Logothetis,et al.  Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex , 2006, PLoS biology.

[66]  S. Bentin,et al.  Processing specificity for human voice stimuli: electrophysiological evidence , 2001, Neuroreport.

[67]  Robert Oostenveld,et al.  Identifying Object Categories from Event-Related EEG: Toward Decoding of Conceptual Representations , 2010, PloS one.

[68]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[69]  R. Näätänen,et al.  Semantic processing in comatose patients with intact temporal lobes as reflected by the N400 event-related potential , 2010, Neuroscience Letters.

[70]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[71]  M. Schaller,et al.  From evidence to clinical practice: effective implementation of therapeutic hypothermia to improve patient outcome after cardiac arrest. , 2006, Critical care medicine.

[72]  Jeroen J. A. van Boxtel,et al.  Opposing effects of attention and consciousness on afterimages , 2010, Proceedings of the National Academy of Sciences.

[73]  M. Murray,et al.  Generating Controlled Image Sets in Cognitive Neuroscience Research , 2008, Brain Topography.