In the current study we conducted two experiments with auditory pitch deviance and measured the OMI response. We found that when the deviant was frequent and therefore predictable, microsaccade inhibition onset was faster as a function of the deviant size (higher pitch) and when it was rare, the inhibition was prolonged. This was achieved without the observer’s response. Next, we will discuss the different aspects of these findings and their interpretation.
Auditory deviance and OMI: salience vs. surprise
Given that an auditory oddball was found to increase the period of saccadic inhibition, i.e., postpone its release, at least when a task was involved 4,17, one would expect that this inhibition will be prolonged with a larger deviance. On the other hand, since the OMI is known to be faster and shorter with the saliency of the stimuli, e.g., for higher visual contrast 6, one would expect faster and shorter inhibition with a larger deviance that appears perceptually more salient.
In experiment 1, the stimulus was a repeated short sequence of 5 identical tones, or it contained a fifth deviant tone. The deviant was fixed within a condition and varied between conditions; in this way, the deviant was frequent and totally predictable. We found that the OMI was sensitive to the auditory pitch deviance and was affected by its magnitude. In response to a larger deviance, the OMI was faster (started earlier) as evident by the difference in the rate modulation function (Figure 3b) and by the earlier inhibition onset around the time of the deviant tone presentation (Figure 3c). Because the deviant was predictable, the results resemble those of the OMI in response to visual contrast stimuli 6 that show a faster inhibition onset for higher contrast. Here, the effect of the deviant tone did not stem from an unpredictable change or surprise, but instead from its contrast with the 4 preceding standard tones, hence, the similarity to the effect of visual contrast. We therefore can conclude that the OMI measured in this experiment reflects the perceived stimulus saliency.
The results of this experiment could be explained by referring to two early processes of change detection in the auditory modality, originating from the auditory cortex and biasing attention away from the common stimulus. Stimulus Specific Adaptation (SSA) and Mismatch Negativity (MMN) are not entirely dissociated, and some studies suggested that SSA provides a neuronal correlate of MMN 31,32. Stimulus Specific Adaptation (SSA) reflects the habituation to a recurring stimulus, spanning several time scales ranging from milliseconds to tens of seconds 33. The evoked potential (ERP) Mismatch Negativity (MMN) reflects the brain’s response to a sudden change in stimulus, peaking at about 150ms 34–36. Based on these known processes, we considered the following explanation of our results: Early inhibition onset indicates preparation and is associated with temporal anticipation due to the paradigm’s design. A higher sensory saliency of the deviant sequence is caused by habituation of the repetitive reference tone (SSA) and a fresh response to the deviant tone (depending on its deviance 37), resulting in faster inhibition onsets. In addition, the mismatched deviant tone signals a prediction error relative to the size of the difference, leading to a better adjustment of a temporal model 38.
In experiment 2 we used an oddball paradigm, where an infrequent sequence of tones was presented randomly among 6 repeated identical tone sequences at a ratio of 20/80. The results showed that a rare auditory pattern induced a significant surprise response, with a prolonged OMI as in previous oddball studies4,17,20 . With a long inter-stimulus interval (ISI) of two and a half seconds, this effect became non-significant (p=0.05, 2-tailed paired t-test) (Figure 4e). This might be associated with a reduction in alertness due to the slow pace of the experiment, together with the lack of any attentive task. The results indicate a surprise response reflected by prolonged inhibition; however, it could also be associated with early change detection processes as well as an additional top-down re-direction of attention. A late ERP component is associated with attention shifts; P3a is a subcomponent of the P300 complex, which reflects the top-down response to violations of expectations and decision making 39. It occurs 150ms later than MMN peaking, around ~300ms and requires a detection task. Since microsaccade inhibition covaries with spatial attention 25,40,41 and it was reported to be induced by the allocation of spatial attention to the fixation location in the visual field 15,42, we believe that top-down and bottom-up attention re-orientation mechanisms account for the prolonged inhibition.
Note that due to the limited constraints derived from our results, this is not the only reasonable explanation and alternative explanations could also be considered; however, they are left for future work.
The effect of Inter Stimulus Intervals on OMI
We also observed a significant increase in the microsaccade rate as a function of ISI (Figure 5a). This could be explained by reduced alertness and it could result from reduced inhibition in the longer ISIs due to a lower stimulus rate. The link between alertness and microsaccade inhibition was demonstrated, for example, in the finding of reduced inhibition in ADHD in a continuous performance task, which was recovered by administering a stimulating medication10. It was also reported that higher attentional loads, as in the shorter ISIs with increased alertness, are associated with a lower microsaccade rate 43. An alternative explanation may be related to the microsaccade preparation time; there is less time to prepare in the shorter intervals, resulting in fewer microsaccades. Both explanations could be supported by the highly significant longer msRTs in the 0.5sec ISI condition (F(4,160)=5.39 p=0.0004).
Comparison with previous Oddball studies
Previous OMI studies of auditory oddballs 4 involved a task that could have influenced the results by generating an attention effect. For example, our preliminary results from a serial dependency study, in which participants were asked to count a colored patch from a group of red and green patches, showed a significantly longer OMI for the attended stimuli 21. A task such as counting the oddballs 4 involves additional processing time to hold the current number of oddballs within working memory (WM) 44 and to make a decision involving target discrimination. Thus, it could have prolonged the saccadic inhibition for targets regardless of whether or not these targets were oddballs. In our study, the participants were asked to attend to all sounds without any request to pay specific attention to the oddballs in a passive attentive way. We show here, for the first time, the OMI effects for auditory oddballs in a passive attentive paradigm (see 23,24 for a similar passive-attentive paradigm). However, these OMI effects appear smaller than those obtained with attended stimuli 4 or in response to visual stimuli as a function of contrast 6.
Our study implements an auditory oddball paradigm similar to that of Bekinschtein et al. 23, which measured the ERP markers of violations of auditory regularities, either “local” in time, within a single trial (similar to our exp1), or “global” across trials of several seconds (similar to our exp2). Their Local-Global paradigm suggests the existence of a hierarchical organization consisting of at least two levels of perceptual prediction mechanisms: (1) an early mechanism, reflected in the MMN signal, which is effective only in a limited time window for changes that are “local” in time 45, and (2) a later, more distributed predictive mechanism, reflected by P3b (a second subcomponent of P300) response to more “global” violations of expectations 2. They report a global effect as a marker of awareness for a rare auditory pattern with an ISI of ~1.5 seconds, measured by P3b when participants were asked to count the oddballs. In contrast, when participants were engaged in mind-wandering or in an active visual target detection of letters, the P3b magnitude for the surprise sounds decreased dramatically 23. Thus, it follows that in this study the P3b signal could have resulted from counting rather than as a marker of predictive violation because P3b is also related to context updating and is associated with memory operations 46 as holding the number of oddball occurrences in working memory. When we compared our results to this ERP study 23, we found both similarities and differences. Unlike Bekinschtein et al., we did not find an OMI effect for the reversed combination of a global standard (AAAAB) and a global deviant (AAAAA), which implies a strong contribution of early mechanisms to the oddball OMI effect (data not shown). Our participants reported being aware of the oddballs when asked after the experiment; however, their level of engagement and its contribution to the OMI are unknown. It is therefore impossible to distinguish between the contribution of an automatic change detection process and a higher-level predictive mechanism.