Processing of Auditory Novelty Across the Cortical Hierarchy: An Intracranial Electrophysiology Study

Abstract

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.

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

“…For example, evidence suggests that clinical evaluation alone is insufficient to fully evaluate patients with disorders of consciousness (Bayne et al, 2017; Bernat, 2017; Naccache, 2017; Schnakers et al, 2009). The present study also serves as a foundation for ongoing and future studies that seek to gain better understanding of sensitivity of auditory cortical novelty processing to general anesthesia (Nourski et al, 2018). In turn, knowledge gained from this work will contribute to improvements in accuracy of assessing conscious processing in clinical and non-clinical settings.…”

“…The data presented here were collected within the context of a larger study on effects of general anesthesia on auditory cortical responses during a pre-drug baseline period (Nourski et al, 2018). As part of that study, the subjects’ overall level of alertness was evaluated over the course of the experiment using the Observer’s Assessment of Alertness/Sedation (OAA/S) scale, which ranges from OAA/S = 5 for fully awake to OAA/S = 1 for unresponsive even to noxious stimuli (Chernik et al, 1990).…”

Cortical functional connectivity indexes arousal state during sleep and anesthesia

“…Although no specific instructions were given about keeping eyes open or closed, subjects were observed to have eyes closed during nearly all resting state recordings. Data were recorded in 6-minute blocks, interleaved with an auditory stimulus paradigm as part of a separate study (Nourski et al, 2018a, b). Data were collected during an awake baseline period and during induction of general anesthesia with incrementally titrated propofol infusion (50 – 150 μg/kg/min; Supplementary Fig.…”

Cortical encoding of melodic expectations in human temporal cortex

“…Melodic expectations modulate auditory responses in higher cortical areas. Since melodic expectations reflect regularities within a musical tone sequence at multiple time-scales that depend on the extent of knowledge and exposure of the subject listening to them, we hypothesized that neural signals correlated with the melodic properties of the music would be generated at higher hierarchical cortical levels than those strictly due to the acoustics (Sammler et al 2013;Bianco et al 2016;Nourski et al 2018). EEG lacks the spatial resolution needed to test this hypothesis, but the test was possible in spatially localized ECoG recordings from three patients who had electrodes over the early primary auditory areas in the anterior transverse temporal gyrus, also called Heschl Gyrus (HG; patients 1 and 3), the belt regions along planum temporale (PT) and the superior temporal gyrus (STG), as well as the supra-marginal gyrus (SMG) in the parietal lobe (see Tables S1-S3 for details on the channel locations).…”