Interactions between "what" and "when" in the auditory system: temporal predictability enhances repetition suppression

Abstract

Neural activity in the auditory system decreases with repeated stimulation, matching stimulus probability in multiple timescales. This phenomenon, known as stimulus-specific adaptation, is interpreted as a neural mechanism of regularity encoding aiding auditory object formation. However, despite the overwhelming literature covering recordings from single-cell to scalp auditory-evoked potential (AEP), stimulation timing has received little interest. Here we investigated whether timing predictability enhances the experience-dependent modulation of neural activity associated with stimulus probability encoding. We used human electrophysiological recordings in healthy participants who were exposed to passive listening of sound sequences. Pure tones of different frequencies were delivered in successive trains of a variable number of repetitions, enabling the study of sequential repetition effects in the AEP. In the predictable timing condition, tones were delivered with isochronous interstimulus intervals; in the unpredictable timing condition, interstimulus intervals varied randomly. Our results show that unpredictable stimulus timing abolishes the early part of the repetition positivity, an AEP indexing auditory sensory memory trace formation, while leaving the later part (≈ >200 ms) unaffected. This suggests that timing predictability aids the propagation of repetition effects upstream the auditory pathway, most likely from association auditory cortex (including the planum temporale) toward primary auditory cortex (Heschl's gyrus) and beyond, as judged by the timing of AEP latencies. This outcome calls for attention to stimulation timing in future experiments regarding sensory memory trace formation in AEP measures and stimulus probability encoding in animal models.

Figure 1.

Schematic diagram of the roving standard frequency paradigm used in this study. Trains of three, six, or 12 equal tones were randomly delivered without intertrain pauses, with tone frequency varying from 880 to 2921 Hz across trains. In this arrangement, the first tone of a train acts as a low-probability stimulus compared with the previous train [deviant stimulus (DEV); black hexagons], whereas the last tone of a train acts as a high-probability stimulus inside that train [standard stimulus (STD); white hexagons]. A, Predictable timing condition. The SOA and the ITI were set constant at 708 ms. B, Unpredictable timing condition. The SOA varied pseudorandomly between 364 and 1062 ms in seven steps of 118 ms, with the constraint that the SOA previous to the last stimulus in a train as well as the ITI were always 708 ms (asterisks).

Figure 2.

A, Grand-average waveforms for standard (STD), deviant (DEV), and deviant minus standard differences (DEV-STD DW) in predictable (top) and unpredictable (bottom) timing conditions, separately for trains of three (blue trace), six (red trace), and 12 (green trace) tone presentations, as recorded from Fz electrode. Shaded areas indicate SEM. B, P50 amplitudes in predictable (PT) and unpredictable (UT) timing conditions elicited to standard (white circles) and deviant (black circles) stimuli separately for trains of three, six, and 12 tones (amplitudes in microvolts; error bars denote SEM). P50 amplitude increased with repetition only in the predictable timing condition regardless of stimulus type. C, Same as B, but for N1 amplitudes, which were overall larger for deviant than standard stimuli but decreased with further repetition only for standard stimuli in the predictable timing condition. D, Same as B, but for P2 amplitudes elicited to the standard stimulus. P2 amplitudes increased with tone repetition regardless of timing predictability. E, Same as B, but for amplitudes retrieved in a time window around the MMN. Deviant stimuli elicited more negative amplitudes in the MMN time window (MMNwin) than standard stimuli, but only the latter were affected by repetition, an effect manifested as an increase of positivity, larger in the predictable than the unpredictable timing condition.

Figure 3.

A, RP grand-average difference waveforms [AEP to the 12th minus the third standard (STD) stimulus] for predictable (PT; blue trace) and unpredictable (UT; red trace) timing conditions at Fz electrode. Whereas the shape of the RP waveform is similar in both traces, the onset of the significant repetition-related positivity is ∼100 ms earlier in the predictable (blue arrow at the P50 time window, 70 ms) versus the unpredictable (red arrow at the P2 time window, 170 ms) timing condition. B, RP scalp potential distributions at 70, 110, and 170 ms for predictable and unpredictable timing conditions. Note how the development of the frontocentral repetition-related positivity takes place at an earlier latency when stimulation timing is predictable. C, MMN scalp potential distribution after three, six, and 12 tone presentations in predictable and unpredictable timing conditions. Note the repetition-related increase in amplitude and the typical frontocentral distribution of the MMN (using linked mastoids reference).