Processing of auditory novelty across the cortical hierarchy: An intracranial electrophysiology study

• Published in: NeuroImage (Orlando, Fla.) Vol. 183; pp. 412 - 424
• Main Authors: Nourski, Kirill V., Steinschneider, Mitchell, Rhone, Ariane E., Kawasaki, Hiroto, Howard, Matthew A., Banks, Matthew I.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2018; Elsevier Limited
• Subjects: Adult; Auditory Cortex - physiology; Auditory Perception - physiology; Auditory stimuli; Averaged evoked potential; Coding; Consciousness; Convulsions & seizures; Cortex (auditory); Drug Resistant Epilepsy - physiopathology; Drug Resistant Epilepsy - surgery; Electrocorticography; Electrocorticography - methods; Electrophysiology; Evoked Potentials, Auditory - physiology; Female; Firing pattern; Gamma Rhythm - physiology; High gamma; Human auditory cortex; Humans; Hypotheses; Information processing; Latency; Male; Middle Aged; Neurosurgery; Predictive coding; Prefrontal cortex; Sensory integration; Somatosensory cortex; Spatial distribution; Superior temporal gyrus; Temporal cortex; Temporal gyrus; Time Factors; Young Adult; FF; PP; MTG; RT; OAA/S; PT; MRI; High gamma; LS; STG; MNI; HGAL; PFC; ERBP; GD; HGPM; Electrocorticography; LGD; AEP; GS; ROI; Human auditory cortex; MMN; CT; ECoG; Predictive coding; LD; Averaged evoked potential; FB; HG
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2018.08.027

Under the predictive coding hypothesis, specific spatiotemporal patterns of cortical activation are postulated to occur during sensory processing as expectations generate feedback predictions and prediction errors generate feedforward signals. Establishing experimental evidence for this information flow within cortical hierarchy has been difficult, especially in humans, due to spatial and temporal limitations of non-invasive measures of cortical activity. This study investigated cortical responses to auditory novelty using the local/global deviant paradigm, which engages the hierarchical network underlying auditory predictive coding over short (‘local deviance’; LD) and long (‘global deviance’; GD) time scales. Electrocorticographic responses to auditory stimuli were obtained in neurosurgical patients from regions of interest (ROIs) including auditory, auditory-related and prefrontal cortex. LD and GD effects were assayed in averaged evoked potential (AEP) and high gamma (70–150 Hz) signals, the former likely dominated by local synaptic currents and the latter largely reflecting local spiking activity. AEP LD effects were distributed across all ROIs, with greatest percentage of significant sites in core and non-core auditory cortex. High gamma LD effects were localized primarily to auditory cortex in the superior temporal plane and on the lateral surface of the superior temporal gyrus (STG). LD effects exhibited progressively longer latencies in core, non-core, auditory-related and prefrontal cortices, consistent with feedforward signaling. The spatial distribution of AEP GD effects overlapped that of LD effects, but high gamma GD effects were more restricted to non-core areas. High gamma GD effects had shortest latencies in STG and preceded AEP GD effects in most ROIs. This latency profile, along with the paucity of high gamma GD effects in the superior temporal plane, suggest that the STG plays a prominent role in initiating novelty detection signals over long time scales. Thus, the data demonstrate distinct patterns of information flow in human cortex associated with auditory novelty detection over multiple time scales. •Local deviance effects are more broadly distributed than global effects.•Local deviance effects have the shortest onset latencies in core auditory cortex.•Local deviance effect latencies become longer along the auditory cortical hierarchy.•Global deviance effects have the shortest onset latencies in lateral temporal cortex.