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.

AUTHORS

• S. Durschmid

• Erik Edwards

• Christoph Reichert

• Callum Dewar

• Hermann Hinrichs

• Hans-Jochen Heinze

• Heidi E. Kirsch

• Sarang S. Dalal

• Leon Y. Deouell

• Robert T. Knight

Date: 2016

DOI: 10.1073/pnas.1525030113

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Amygdala and Orbitofrontal engagement in breach and resolution of expectancy - a case study

ABSTRACT

Humans constantly predict their environment to facilitate mutual interaction. Predictions are connected with emotions as nonfatal penalties and rewards (for incorrect and correct expectancies, respectively) that result in negative and positive emotions. Music is an ideal stimulus to explore the underlying neurophysiological mechanisms of prediction related emotions. Using the high spatial and temporal resolution of stereotactic depth electrodes, we identified activation patterns and examined their distribution in the bilateral Amygdalae and the orbitofrontal cortex (OFC). We used music excerpts with either (a) a deceptive cadence (i.e., an unexpected chord/breach) or (b) a tonic chord inserted instead of a deceptive cadence (regular chord/no breach). These events were followed by a chord progression leading to and ending on the tonic after a breach (c) or (d) on a tonic after no breach. We computed the differences of the analytic amplitudes in the theta band at these time-points (i.e., events a–d) by using t tests. We found a significant difference between the unexpected chord (a) and the expected chord (b) in the analytic amplitude of the theta band in the left amygdala. Further we found a difference between the 2 resolutions (c and d) in the analytic amplitude of the theta band within the OFC. In conclusion, our case study supports the notion that the amygdala and the OFC are important for emotional responses to musical expectancy breaches as well as of their resolution. (PsycINFO Database Record (c) 2016 APA, all rights reserved)

AUTHORS

• Christian Mikutta

• S. Durschmid

• Nelson Bean

• Moritz Lehne

• James Lubell

• Andreas Altorfer

• Josef Parvizi

• Werner K. Strik

• Robert T. Knight

• Stefan Koelsch

Date: 2015

DOI: dx.doi.org/10.1037/pmu0000121

Sensory Deviancy Detection Measured Directly Within the Human Nucleus Accumbens

Authors:

• S. Durschmid

• Tino Zauhle

• Hermann Hinrichs

• Hans-Jochen Heinze

• Jürgen Voges

• Marta Garrido

• Raymond J. Dolan

• Robert T. Knight

Date: 2015

DOI: 10.1093/cercor/bhu304

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Abstract:

Rapid changes in the environment evoke a comparison between expectancy and actual outcome to inform optimal subsequent behavior. The nucleus accumbens (NAcc), a key interface between the hippocampus and neocortical regions, is a candidate region for mediating this comparison. Here, we report event-related potentials obtained from the NAcc using direct intracranial recordings in 5 human participants while they listened to trains of auditory stimuli differing in their degree of deviation from repetitive background stimuli. NAcc recordings revealed an early mismatch signal (50–220 ms) in response to all deviants. NAcc activity in this time window was also sensitive to the statistics of stimulus deviancy, with larger amplitudes as a function of the level of deviancy. Importantly, this NAcc mismatch signal also predicted generation of longer latency scalp potentials (300–400 ms). The results provide direct human evidence that the NAcc is a key component of a network engaged in encoding statistics of the sensory environmental.

Oscillatory dynamics track motor learning in human cortex

Authors:

• S. Durschmid

• Fanny Quandt

• Ulrike M. Krämer

• Hermann Hinrichs

• R. T. Schultz

• H. Pannek

• Edward F. Chang

• Robert T. Knight

Date: 2014

DOI: 10.1371/journal.pone.0089576

PubMed: 24586885

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Abstract:

Improving performance in motor skill acquisition is proposed to be supported by tuning of neural networks. To address this issue we investigated changes of phase-amplitude cross-frequency coupling (paCFC) in neuronal networks during motor performance improvement. We recorded intracranially from subdural electrodes (electrocorticogram; ECoG) from 6 patients who learned 3 distinct motor tasks requiring coordination of finger movements with an external cue (serial response task, auditory motor coordination task, go/no-go). Performance improved in all subjects and all tasks during the first block and plateaued in subsequent blocks. Performance improvement was paralleled by increasing neural changes in the trial-to-trial paCFC between theta ([Formula: see text]; 4-8 Hz) phase and high gamma (HG; 80-180 Hz) amplitude. Electrodes showing this covariation pattern (Pearson's r ranging up to .45) were located contralateral to the limb performing the task and were observed predominantly in motor brain regions. We observed stable paCFC when task performance asymptoted. Our results indicate that motor performance improvement is accompanied by adjustments in the dynamics and topology of neuronal network interactions in the [Formula: see text] and HG range. The location of the involved electrodes suggests that oscillatory dynamics in motor cortices support performance improvement with practice.

Phase-amplitude cross-frequency coupling in the human nucleus acumbens tracks action monitoring during cognitive control

Authors:

• S. Durschmid

• Tino Zaehle

• Klaus Kopitzki

• Jürgen Voges

• Friedhelm Schmitt

• Hans-Jochen Heinze

• Robert T. Knight

• Hermann Hinrichs

Date: 2013

DOI: 10.3389/fnhum.2013.00635

PubMed: 24586885

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Abstract:

The Nucleus Accumbens (NAcc) is an important structure for the transfer of information between cortical and subcortical structures, especially the prefrontal cortex and the hippocampus. However, the mechanism that allows the NAcc to achieve this integration is not well understood. Phase-amplitude cross-frequency coupling (PAC) of oscillations in different frequency bands has been proposed as an effective mechanism to form functional networks to optimize transfer and integration of information. Here we assess PAC between theta and high gamma oscillations as a potential mechanism that facilitates motor adaptation. To address this issue we recorded intracranial field potentials directly from the bilateral human NAcc in three patients while they performed a motor learning task that varied in the level of cognitive control needed to perform the task. As in rodents, PAC was observable in the human NAcc, transiently occurring contralateral to a movement following the motor response. Importantly, PAC correlated with the level of cognitive control needed to monitor the action performed. This functional relation indicates that the NAcc is engaged in action monitoring and supports the evaluation of motor programs during adaptive behavior by means of PAC.

High gamma oscillations in ECoG allow for pre-movement decoding of dextrous finger movements.

Authors:

• Fanny Quandt

• S. Durschmid

• Hermann Hinrichs

• Robert T. Knight

• Jochem W. Rieger

Date: 2012