Involuntary orienting of attention to a sound desynchronizes the occipital alpha rhythm and improves visual perception

Highlights

• Peripheral sounds elicit lateralized desynchronization of the occipital alpha rhythm.

• Sound-induced alpha desynchronization strongly predicts visual discrimination accuracy.

• Lateralized alpha desynchronization reflects the involuntary orienting of attention.

• Alpha modulations for involuntary attention differ from voluntary attention.

Abstract

Directing attention voluntarily to the location of a visual target results in an amplitude reduction (desynchronization) of the occipital alpha rhythm (8–14 Hz), which is predictive of improved perceptual processing of the target. Here we investigated whether modulations of the occipital alpha rhythm triggered by the involuntary orienting of attention to a salient but spatially non-predictive sound would similarly influence perception of a subsequent visual target. Target discrimination was more accurate when a sound preceded the target at the same location (validly cued trials) than when the sound was on the side opposite to the target (invalidly cued trials). This behavioral effect was accompanied by a sound-induced desynchronization of the alpha rhythm over the lateral occipital scalp. The magnitude of alpha desynchronization over the hemisphere contralateral to the sound predicted correct discriminations of validly cued targets but not of invalidly cued targets. These results support the conclusion that cue-induced alpha desynchronization over the occipital cortex is a manifestation of a general priming mechanism that improves visual processing and that this mechanism can be activated either by the voluntary or involuntary orienting of attention. Further, the observed pattern of alpha modulations preceding correct and incorrect discriminations of valid and invalid targets suggests that involuntary orienting to the non-predictive sound has a rapid and purely facilitatory influence on processing targets on the cued side, with no inhibitory influence on targets on the opposite side.

Introduction

Attending to a stimulus in one modality facilitates the processing of stimuli in other modalities that occur at the location of the attended stimulus (Calvert et al., 2004, Murray and Wallace, 2012). Such cross-modal facilitation has been observed not only when observers voluntarily direct attention in response to an instructional cue (e.g., a directional arrow) but also when a salient, but otherwise irrelevant, environmental event attracts attention to its location involuntarily (McDonald et al., 2012, McDonald et al., 2013a, McDonald and Ward, 2000, Spence and Driver, 2004). For example, a sudden noise burst to the left or right of the midline can facilitate speeded responses to nearby visual targets (McDonald and Ward, 2000, Spence and Driver, 1997) and enhance the perceptual processing of visual targets at the cued location (Dufour, 1999, Feng et al., 2014, McDonald et al., 2000, McDonald et al., 2005, Störmer et al., 2009), even when the noise burst does not predict the target's location.

Recently, McDonald and colleagues (McDonald et al., 2013b) found that non-predictive auditory cues elicit a slow event-related potential (ERP) shift with an amplitude maximum over the visual cortex contralateral to the side of the sound. The magnitude of this auditory-evoked contralateral occipital positivity (termed the ACOP) was found to predict the perceived contrast of a subsequent visual target (McDonald et al., 2013b) and the accuracy of its discrimination (Feng et al., 2014). The ACOP closely resembles slow-wave ERP activity triggered by voluntary shifts of visual attention (in particular, the late directing attention positivity or LDAP; Harter et al., 1989; Hopf and Mangun, 2000; McDonald et al., 2013b; Nobre et al., 2000), except that the ACOP is elicited considerably earlier in time. Thus, it was proposed that the ACOP is a neural signature of the involuntary, rapid orienting of visual attention to the location of a salient sound (Hillyard et al., 2016, McDonald et al., 2013a, McDonald et al., 2013b). Matusz et al. (2016) reported that infrequent auditory deviants delivered via earphones elicit the ACOP under passive-listening conditions, but only when location of the deviant is unpredictable. These results suggest that the cross-modal activation of visual cortex is reflexive but not entirely automatic (i.e., it is not obligatory).

In addition to slow-wave ERP activity over the posterior scalp, the voluntary orienting of visual-spatial attention is accompanied by strong modulations of the ongoing occipital alpha rhythm (8–14 Hz) in the cue-target interval. In a widely studied spatial attention paradigm, attention is directed to the left or right visual half-field by a symbolic cue (e.g., a central arrow), which is followed by a target stimulus to be detected or discriminated in either the cued or the uncued hemifield. Alpha power measured in the cue-target interval is typically decreased over the hemisphere contralateral to the attended side, with a lesser decrease or even an increase over the hemisphere ipsilateral to the attended side (for reviews, see Banerjee et al., 2011; Foxe and Snyder, 2011; Hanslmayr et al., 2011; Ikkai et al., 2016; Jensen and Mazaheri, 2010; Klimesch, 2012; Payne and Sekuler, 2014; Thut et al., 2012). The decreased (desynchronized) alpha rhythm over the contralateral hemisphere has been linked with improved processing of the attended-field stimulus, whereas the relative increase in ipsilateral alpha power has been considered a sign of the active suppression of distracting inputs from the unattended visual half-field (Green and McDonald, 2010, Kelly et al., 2006, Händel et al., 2011, Okazaki et al., 2014, Payne et al., 2013, Rihs et al., 2007, Rihs et al., 2009, Sauseng et al., 2005, Worden et al., 2000). Consistent with these findings, decreased alpha amplitudes have been correlated with improved perceptual processing of visual events at voluntarily attended locations in a wide variety of tasks (e.g., Ergenoglu et al., 2004; Gould et al., 2011; Hanslmayr et al., 2007; Kelly et al., 2009; Mazaheri et al., 2014; Romei et al., 2008; Thut et al., 2006, Thut et al., 2012; Trenner et al., 2008; van Dijk et al., 2008; Yamagishi et al., 2008).

While the foregoing studies have demonstrated a strong linkage between the voluntary allocation of visual-spatial attention and modulation of the occipital alpha rhythm, little is known about modulations of the alpha rhythm that accompany the involuntary orienting of attention or whether such modulations have an effect on perceptual processing. Behavioral studies over the past four decades have drawn a fundamental distinction between the voluntary (top-down or endogenous) orienting of attention to a target's location by a symbolic cue and the involuntary (bottom-up, exogenous or automatic) capture of attention by a salient physical event that is not informative regarding the target's location (Briand, 1998, Jonides, 1980, Müller and Rabbitt, 1989, Posner and Cohen, 1984; reviewed in Wright and Ward (2008)). Voluntary and involuntary orienting of attention differ in several important properties. Whereas voluntary orienting proceeds slowly and may be sustained over periods of one to several seconds, involuntary orienting is transient, with a rapid onset and a transition into an inhibitory phase (inhibition of return) after several hundred milliseconds. Involuntary attention is also less sensitive to concurrent task interference and to the predictability of target location by the cue. Neuroimaging studies indicate that these two forms of attention are mediated by different neural networks (Corbetta and Shulman, 2002, Kincade et al., 2005, Mayers et al., 2004; reviewed in Santangelo et al. (2009)).

Previous studies have reported that the involuntary orienting of attention to a lateralized vibrotactile (Trenner et al., 2008) or auditory (Mlynarski et al., 2014, Störmer et al., 2016) stimulus is associated with a sharp decrease of the occipital alpha rhythm that is more pronounced over the hemisphere contralateral to the stimulus location. However, it remains unclear whether such involuntary modulations of the occipital alpha rhythm have any impact upon perceptual processing of visual events. The present study investigates this question in the cross-modal cueing paradigm previously described by Feng et al. (2014), in which a peripheral sound cue was followed after 400 ms by a masked letter (T or L) presented unpredictably to the same or opposite side as the sound (see Fig. 1). One advantage of using an auditory (rather than a visual) cue to examine attention effects on the occipital alpha rhythm is the absence of a visual evoked potential elicited by the cue, which typically contains alpha-band activity that may confound measurements of attention-related alpha modulations in the cue-target interval. To preview the present results, we found that contralateral alpha desynchronization associated with the involuntary orienting of attention to the sound was highly predictive of accurate visual perception, but only when the targets appeared on the same side as the sound (i.e., when targets were validly cued).