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 (ϳϾ200 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.

Similar sound intensity dependence of the N1 and P2 components of the auditory ERP: Averaged and single trial evidence

“…Recent research has focused on different strategies for disentangling N1 from P2. For example, temporal unpredictability of stimulus occurrence, when compared with fixed inter-stimulus intervals (Pereira et al, 2014), induced differential modulations in N1 and P2 components (Costa-Faidella et al, 2011). Likewise, the presentation of human vocal auditory stimuli induced higher P2 component amplitudes with no effects on the N1 component (Charest et al, 2009).…”

Cortical oscillations and sensory predictions

“…In the absence of such a phase reset or if stimuli occur in a non-ideal phase, behavioral responses are suppressed or slowed down. (c) When the timing of a sound is correctly anticipated (right panel), a decrease in evoked auditory responses (N1) is observed [22,23]. This schematic compares the amplitude of an event-related response (N1, averaged across 10 trials) to unexpected (left panel) and expected (right panel) auditory stimuli.…”

“…The predictive alignment of delta-theta oscillations in an ideal excitability phase speeds up stimulus detection (Figure 1b) [20,21]. Furthermore, when stimuli are implicitly expected based on their temporal regularity, early sensory responses are reduced (Figure 1c) [22,23]. The magnitude of neural responses, however, depends on whether temporal predictions are tested in the presence or absence of explicit attention to the nature or location of those events (Box 1 and [24][25][26][27]).…”

“…In these theories, internal models make it possible to infer either (i) forthcoming sensory input or (ii) the sensory consequences of an action. When experimentally tested, both types of inference are associated with reduced evoked responses relative to responses to unexpected sensory inputs [22,95]. In the context of action, response reduction relies on efference copies propagating from motor to sensory cortices [95].…”

Encoding of event timing in the phase of neural oscillations

“…The lack of repetition suppression in both sensory cortices may thus be an index of successful attentional orienting. Additionally, recent findings have shown that the more temporally predictable, the higher the repetition suppression effects notably in the auditory responses (Costa-Faidella et al, 2011;Summerfield et al, 2008Summerfield et al, , 2011. In the context of predictive coding models, it has also been suggested that repetition and expectation were dissociable (Todorovic and de Lange, 2012).…”