Hierarchy of prediction errors for auditory events in human temporal and frontal cortex

Abstract

Predictive coding theories posit that neural networks learn statistical regularities in the environment for comparison with actual outcomes, signaling a prediction error (PE) when sensory deviation occurs. PE studies in audition have capitalized on low-frequency event-related potentials (LF-ERPs), such as the mismatch negativity. However, local cortical activity is well-indexed by higher-frequency bands [high-γ band (Hγ): 80-150 Hz]. We compared patterns of human Hγ and LF-ERPs in deviance detection using electrocorticographic recordings from subdural electrodes over frontal and temporal cortices. Patients listened to trains of task-irrelevant tones in two conditions differing in the predictability of a deviation from repetitive background stimuli (fully predictable vs. unpredictable deviants). We found deviance-related responses in both frequency bands over lateral temporal and inferior frontal cortex, with an earlier latency for Hγ than for LF-ERPs. Critically, frontal Hγ activity but not LF-ERPs discriminated between fully predictable and unpredictable changes, with frontal cortex sensitive to unpredictable events. The results highlight the role of frontal cortex and Hγ activity in deviance detection and PE generation.predictive coding | prediction error | mismatch negativity | frontal cortex | high γ-activity

Evaluating the neurophysiological evidence for predictive processing as a model of perception

“…If gamma‐band oscillations represent the output of error units, unpredictable deviants would be expected to provoke strong gamma‐band activity, while predictable deviants should elicit a more muted response. Although Durschmid et al 182 . did find that high‐gamma (>60 Hz) responses differentiated between unpredictable and predictable deviant tones at frontal sites, unpredictable and predictable deviants elicited equivalent high‐gamma activity over temporal cortex.…”

“…Accordingly, early responses to local deviants are typically confined to primary sensory cortex, while violations of complex regularities evoke activity across distributed, higher‐level areas (e.g., Ref. 182; see Ref. 42 for a review).…”

Deviance detection is the dominant component of auditory contextual processing in the lateral superior temporal gyrus: A human ECoG study

“…Although little difference was seen between the mismatch response of the frontal lobe and that of STG for “predictable” stimuli, significantly stronger response of the frontal lobe was detected for “unpredictable” stimuli. That result showed that the frontal lobe was responsible for detecting “prediction errors” (Durschmid et al, ). In our study, although frontal MMR was observed in four of the 10 subjects, neither a consistent localization pattern nor association with MMR was evident in the frontal lobe.…”

Oscillatory Dynamics of Prefrontal Cognitive Control

“…For example, a human intracranial study measuring high frequency neural activity demonstrated that the PFC only became active when unpredicted deviants were detected (Figure 1A, [31]). Neither predicted deviants nor standards elicited any meaningful PFC activation, while sensory areas did not distinguish between predicted and unpredicted deviants.…”

“…Furthermore, different frequency bands allow multiplexing different computations on several temporal scales. The graphs in a and c are reproduced with permission from [31,33]. The graphs in d and e appeared under the Creative Commons Attribution (CC BY) license [28,38].…”