Spatial and temporal relationships of electrocorticographic alpha and gamma activity during auditory processing.
Neuroimaging approaches have implicated multiple brain sites in musical perception, including the posterior part of the superior temporal gyrus and adjacent perisylvian areas. However, the detailed spatial and temporal relationship of neural signals that support auditory processing is largely unknown. In this study, we applied a novel inter-subject analysis approach to electrophysiological signals recorded from the surface of the brain (electrocorticography (ECoG)) in ten human subjects. This approach allowed us to reliably identify those ECoG features that were related to the processing of a complex auditory stimulus (i.e., continuous piece of music) and to investigate their spatial, temporal, and causal relationships. Our results identified stimulus-related modulations in the alpha (8-12 Hz) and high gamma (70-110 Hz) bands at neuroanatomical locations implicated in auditory processing. Specifically, we identified stimulus-related ECoG modulations in the alpha band in areas adjacent to primary auditory cortex, which are known to receive afferent auditory projections from the thalamus (80 of a total of 15,107 tested sites). In contrast, we identified stimulus-related ECoG modulations in the high gamma band not only in areas close to primary auditory cortex but also in other perisylvian areas known to be involved in higher-order auditory processing, and in superior premotor cortex (412/15,107 sites). Across all implicated areas, modulations in the high gamma band preceded those in the alpha band by 280 ms, and activity in the high gamma band causally predicted alpha activity, but not vice versa (Granger causality, p<1e(-8)). Additionally, detailed analyses using Granger causality identified causal relationships of high gamma activity between distinct locations in early auditory pathways within superior temporal gyrus (STG) and posterior STG, between posterior STG and inferior frontal cortex, and between STG and premotor cortex. Evidence suggests that these relationships reflect direct cortico-cortical connections rather than common driving input from subcortical structures such as the thalamus. In summary, our inter-subject analyses defined the spatial and temporal relationships between music-related brain activity in the alpha and high gamma bands. They provide experimental evidence supporting current theories about the putative mechanisms of alpha and gamma activity, i.e., reflections of thalamo-cortical interactions and local cortical neural activity, respectively, and the results are also in agreement with existing functional models of auditory processing.
BCI R&D Program, Wadsworth Center, New York State Department of Health, Albany, NY, USA; Department of Electrical and Computer Engineering, University of Texas at El Paso, TX, USA. Electronic address: cmpotes@gmail.com.
Cristhian
C
Potes
BCI R&D Program, Wadsworth Center, New York State Department of Health, Albany, NY, USA; Department of Neurology, Albany Medical College, Albany, NY, USA; Department of Computer Science, Graz University of Technology, Graz, Austria. Electronic address: pbrunner@wadsworth.org.
Peter
P
Brunner
BCI R&D Program, Wadsworth Center, New York State Department of Health, Albany, NY, USA; Department of Neurology, Albany Medical College, Albany, NY, USA; J. Crayton Pruitt Family, Department of Biomedical Engineering, University of Florida, Gainesville, FL, USA. Electronic address: agunduz@ufl.edu.
Aysegul
A
Gunduz
Department of Psychology, University of California at Berkeley, CA, USA. Electronic address: rtknight@berkeley.edu.
Robert T
RT
Knight
BCI R&D Program, Wadsworth Center, New York State Department of Health, Albany, NY, USA; Department of Electrical and Computer Engineering, University of Texas at El Paso, TX, USA; Department of Neurology, Albany Medical College, Albany, NY, USA; Department of Biomedical Science, State University of NY at Albany, Albany, NY, USA. Electronic address: schalk@wadsworth.org.
Gerwin
G
Schalk
D000161:Acoustic Stimulation; D000293:Adolescent; D000328:Adult; D000513:Alpha Rhythm / Q000502:physiology*; D001307:Auditory Perception / Q000502:physiology*; D001931:Brain Mapping; D015984:Causality; D004569:Electroencephalography / Q000379:methods*; D004827:Epilepsy / Q000523:psychology; D005260:Female; D065818:Gamma Rhythm / Q000502:physiology*; D006801:Humans; D007206:Individuality; D008297:Male; D008875:Middle Aged; D009146:Music / Q000523:psychology; D055815:Young Adult
Alpha and high gamma activity; Auditory processing; Electrocorticography (ECoG); Functional connectivity; Granger causality; Thalamo-cortical interactions