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Implicit learning of predictable sound sequences modulates human brain responses at different levels of the auditory hierarchy.

Lecaignard F, Bertrand O, Gimenez G, Mattout J, Caclin A - Front Hum Neurosci (2015)

Bottom Line: We observed a decrease of the MMN with predictability and interestingly, a similar effect at earlier latencies, within 70 ms after deviance onset.Following these pre-attentive responses, a reduced P3a was measured in the case of predictable deviants.We conclude that early and late deviance responses reflect prediction errors, triggering belief updating within the auditory hierarchy.

View Article: PubMed Central - PubMed

Affiliation: Lyon Neuroscience Research Center, CRNL, INSERM, U1028 - CNRS, UMR5292, Brain Dynamics and Cognition Team Lyon, France ; University Lyon 1 Lyon, France ; MEG Department, CERMEP Imaging Center Lyon, France.

ABSTRACT
Deviant stimuli, violating regularities in a sensory environment, elicit the mismatch negativity (MMN), largely described in the Event-Related Potential literature. While it is widely accepted that the MMN reflects more than basic change detection, a comprehensive description of mental processes modulating this response is still lacking. Within the framework of predictive coding, deviance processing is part of an inference process where prediction errors (the mismatch between incoming sensations and predictions established through experience) are minimized. In this view, the MMN is a measure of prediction error, which yields specific expectations regarding its modulations by various experimental factors. In particular, it predicts that the MMN should decrease as the occurrence of a deviance becomes more predictable. We conducted a passive oddball EEG study and manipulated the predictability of sound sequences by means of different temporal structures. Importantly, our design allows comparing mismatch responses elicited by predictable and unpredictable violations of a simple repetition rule and therefore departs from previous studies that investigate violations of different time-scale regularities. We observed a decrease of the MMN with predictability and interestingly, a similar effect at earlier latencies, within 70 ms after deviance onset. Following these pre-attentive responses, a reduced P3a was measured in the case of predictable deviants. We conclude that early and late deviance responses reflect prediction errors, triggering belief updating within the auditory hierarchy. Beside, in this passive study, such perceptual inference appears to be modulated by higher-level implicit learning of sequence statistical structures. Our findings argue for a hierarchical model of auditory processing where predictive coding enables implicit extraction of environmental regularities.

No MeSH data available.


Related in: MedlinePlus

Deviance effects. (A) Grand-average ERPs (n = 22 participants) elicited by standards just preceding a deviant (solid line), deviants (dotted line) and difference responses (bold solid line) at electrode Fz and TP9 in bandwidth 2–45 Hz for condition UF (left column), PF (middle column), and UI (right column). Main components in standard (N1, P2) and difference responses [mismatch negativity (MMN), P3a] are shown for condition UF. (B) Statistical maps obtained with non-parametric tests (n = 100,000 permutations) when comparing standard and deviant responses, at each electrode and each latency of the whole trial. Three intervals of significance were revealed for unpredictable sequences (UF, UI) at early latencies, and at the latency of the MMN and the P3a whereas only two were observed for condition PF at the latency of the MMN and P3a. Electrodes are sorted by spatial clusters (left column, from top to bottom: LF, left frontal, RF, right frontal, FC, fronto-central, CP, centro-parietal, LT, left temporal, RT, right temporal, PO, parieto-occipital). (C) Scalp topographies of the grand-average difference ERP, at the early effect (left column), the MMN (middle column) and the P3a (right column) latencies, for each condition. The MMN significant (positive) inversion is visible in each condition. Similarly, early deviance effect in condition UF and UI also entail a (negative) inversion but this does not reach significance.
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Figure 2: Deviance effects. (A) Grand-average ERPs (n = 22 participants) elicited by standards just preceding a deviant (solid line), deviants (dotted line) and difference responses (bold solid line) at electrode Fz and TP9 in bandwidth 2–45 Hz for condition UF (left column), PF (middle column), and UI (right column). Main components in standard (N1, P2) and difference responses [mismatch negativity (MMN), P3a] are shown for condition UF. (B) Statistical maps obtained with non-parametric tests (n = 100,000 permutations) when comparing standard and deviant responses, at each electrode and each latency of the whole trial. Three intervals of significance were revealed for unpredictable sequences (UF, UI) at early latencies, and at the latency of the MMN and the P3a whereas only two were observed for condition PF at the latency of the MMN and P3a. Electrodes are sorted by spatial clusters (left column, from top to bottom: LF, left frontal, RF, right frontal, FC, fronto-central, CP, centro-parietal, LT, left temporal, RT, right temporal, PO, parieto-occipital). (C) Scalp topographies of the grand-average difference ERP, at the early effect (left column), the MMN (middle column) and the P3a (right column) latencies, for each condition. The MMN significant (positive) inversion is visible in each condition. Similarly, early deviance effect in condition UF and UI also entail a (negative) inversion but this does not reach significance.

Mentions: Figure 2 displays ERPs (with bandwidth 2–45 Hz) at electrodes Fz and TP9, for the standard, deviant, and difference responses, in each experimental condition. It also shows the statistically significant patterns in the deviance responses and the corresponding scalp topographies at relevant latencies. In every condition, the standards just preceding a deviant elicited a N1 component peaking around 95 ms, associated with a negativity distributed over fronto-central electrodes and followed by a fronto-central P2 component peaking around 155 ms. As shown on Figure 2, testing for deviance effects revealed three significant time-windows for the unpredictable sequences and two for the predictable one: an early time-window (within 70 ms after stimulus onset) for conditions UF and UI, and for the three conditions, we could detect a MMN and a P3a.


Implicit learning of predictable sound sequences modulates human brain responses at different levels of the auditory hierarchy.

Lecaignard F, Bertrand O, Gimenez G, Mattout J, Caclin A - Front Hum Neurosci (2015)

Deviance effects. (A) Grand-average ERPs (n = 22 participants) elicited by standards just preceding a deviant (solid line), deviants (dotted line) and difference responses (bold solid line) at electrode Fz and TP9 in bandwidth 2–45 Hz for condition UF (left column), PF (middle column), and UI (right column). Main components in standard (N1, P2) and difference responses [mismatch negativity (MMN), P3a] are shown for condition UF. (B) Statistical maps obtained with non-parametric tests (n = 100,000 permutations) when comparing standard and deviant responses, at each electrode and each latency of the whole trial. Three intervals of significance were revealed for unpredictable sequences (UF, UI) at early latencies, and at the latency of the MMN and the P3a whereas only two were observed for condition PF at the latency of the MMN and P3a. Electrodes are sorted by spatial clusters (left column, from top to bottom: LF, left frontal, RF, right frontal, FC, fronto-central, CP, centro-parietal, LT, left temporal, RT, right temporal, PO, parieto-occipital). (C) Scalp topographies of the grand-average difference ERP, at the early effect (left column), the MMN (middle column) and the P3a (right column) latencies, for each condition. The MMN significant (positive) inversion is visible in each condition. Similarly, early deviance effect in condition UF and UI also entail a (negative) inversion but this does not reach significance.
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Figure 2: Deviance effects. (A) Grand-average ERPs (n = 22 participants) elicited by standards just preceding a deviant (solid line), deviants (dotted line) and difference responses (bold solid line) at electrode Fz and TP9 in bandwidth 2–45 Hz for condition UF (left column), PF (middle column), and UI (right column). Main components in standard (N1, P2) and difference responses [mismatch negativity (MMN), P3a] are shown for condition UF. (B) Statistical maps obtained with non-parametric tests (n = 100,000 permutations) when comparing standard and deviant responses, at each electrode and each latency of the whole trial. Three intervals of significance were revealed for unpredictable sequences (UF, UI) at early latencies, and at the latency of the MMN and the P3a whereas only two were observed for condition PF at the latency of the MMN and P3a. Electrodes are sorted by spatial clusters (left column, from top to bottom: LF, left frontal, RF, right frontal, FC, fronto-central, CP, centro-parietal, LT, left temporal, RT, right temporal, PO, parieto-occipital). (C) Scalp topographies of the grand-average difference ERP, at the early effect (left column), the MMN (middle column) and the P3a (right column) latencies, for each condition. The MMN significant (positive) inversion is visible in each condition. Similarly, early deviance effect in condition UF and UI also entail a (negative) inversion but this does not reach significance.
Mentions: Figure 2 displays ERPs (with bandwidth 2–45 Hz) at electrodes Fz and TP9, for the standard, deviant, and difference responses, in each experimental condition. It also shows the statistically significant patterns in the deviance responses and the corresponding scalp topographies at relevant latencies. In every condition, the standards just preceding a deviant elicited a N1 component peaking around 95 ms, associated with a negativity distributed over fronto-central electrodes and followed by a fronto-central P2 component peaking around 155 ms. As shown on Figure 2, testing for deviance effects revealed three significant time-windows for the unpredictable sequences and two for the predictable one: an early time-window (within 70 ms after stimulus onset) for conditions UF and UI, and for the three conditions, we could detect a MMN and a P3a.

Bottom Line: We observed a decrease of the MMN with predictability and interestingly, a similar effect at earlier latencies, within 70 ms after deviance onset.Following these pre-attentive responses, a reduced P3a was measured in the case of predictable deviants.We conclude that early and late deviance responses reflect prediction errors, triggering belief updating within the auditory hierarchy.

View Article: PubMed Central - PubMed

Affiliation: Lyon Neuroscience Research Center, CRNL, INSERM, U1028 - CNRS, UMR5292, Brain Dynamics and Cognition Team Lyon, France ; University Lyon 1 Lyon, France ; MEG Department, CERMEP Imaging Center Lyon, France.

ABSTRACT
Deviant stimuli, violating regularities in a sensory environment, elicit the mismatch negativity (MMN), largely described in the Event-Related Potential literature. While it is widely accepted that the MMN reflects more than basic change detection, a comprehensive description of mental processes modulating this response is still lacking. Within the framework of predictive coding, deviance processing is part of an inference process where prediction errors (the mismatch between incoming sensations and predictions established through experience) are minimized. In this view, the MMN is a measure of prediction error, which yields specific expectations regarding its modulations by various experimental factors. In particular, it predicts that the MMN should decrease as the occurrence of a deviance becomes more predictable. We conducted a passive oddball EEG study and manipulated the predictability of sound sequences by means of different temporal structures. Importantly, our design allows comparing mismatch responses elicited by predictable and unpredictable violations of a simple repetition rule and therefore departs from previous studies that investigate violations of different time-scale regularities. We observed a decrease of the MMN with predictability and interestingly, a similar effect at earlier latencies, within 70 ms after deviance onset. Following these pre-attentive responses, a reduced P3a was measured in the case of predictable deviants. We conclude that early and late deviance responses reflect prediction errors, triggering belief updating within the auditory hierarchy. Beside, in this passive study, such perceptual inference appears to be modulated by higher-level implicit learning of sequence statistical structures. Our findings argue for a hierarchical model of auditory processing where predictive coding enables implicit extraction of environmental regularities.

No MeSH data available.


Related in: MedlinePlus