Involuntary Spatial Attention Influences Auditory Processing: Evidence from Human Electrophysiology

Transcription

1 Involuntary Spatial Attention Influences Auditory Processing: Evidence from Human Electrophysiology by Jennifer A. Schneider B. A. (Hons., Psychology), University of Manitoba, 2006 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Arts in the Department of Psychology Faculty of Arts and Social Sciences Jennifer A. Schneider 2012 Simon Fraser University Summer 2012 All rights reserved. However, in accordance with the Copyright Act of Canada, this work may be reproduced, without authorization, under the conditions for Fair Dealing. Therefore, limited reproduction of this work for the purposes of private study, research, criticism, review and news reporting is likely to be in accordance with the law, particularly if cited appropriately.

2 Approval Name: Degree: Jennifer A. Schneider Master of Arts (Psychology) Title of Thesis: Examining Committee: Involuntary Spatial Attention Influences Auditory Processing: Evidence from Human Electrophysiology Chair: Thomas Spalek John McDonald Senior Supervisor Associate Professor Richard Wright Supervisor Associate Professor Matthew Tata External Examiner Associate Professor, Department of Neuroscience University of Lethbridge Date Defended/Approved: July 20, 2012 ii

3 Partial Copyright Licence iii

4 Ethics Statement The author, whose name appears on the title page of this work, has obtained, for the research described in this work, either: or a. human research ethics approval from the Simon Fraser University Office of Research Ethics, b. advance approval of the animal care protocol from the University Animal Care Committee of Simon Fraser University; or has conducted the research or c. as a co-investigator, collaborator or research assistant in a research project approved in advance, d. as a member of a course approved in advance for minimal risk human research, by the Office of Research Ethics. A copy of the approval letter has been filed at the Theses Office of the University Library at the time of submission of this thesis or project. The original application for approval and letter of approval are filed with the relevant offices. Inquiries may be directed to those authorities. Simon Fraser University Library Burnaby, British Columbia, Canada update Spring 2010

5 Abstract The appearance of spatially non-predictive auditory cues can attract attention resulting in facilitation or inhibition of responses to subsequent targets at short or long cue-target intervals, respectively. With most research focusing on visual and crossmodal spatial attention, little is known about the neural mechanisms associated with auditory cue effects. The present study used ERPs to investigate the consequences of involuntary auditory spatial attention on the neural processing of sounds in spatial and non-spatial go/no-go tasks. The negative-difference component which is known to reflect attentional enhancement of target processing was observed in both experiments, indicating that salient, spatially non-predictive auditory cues captured attention. A subsequent positive difference was observed only in the spatial task, suggesting this component corresponds with the presence or absence of RT cue effects in auditory spatial cueing tasks. In both tasks, auditory sounds activated occipital regions, suggesting that visual regions are involved in processing auditory stimuli. Keywords: Event-related potentials; auditory spatial attention; difference waveforms; visual cortex iv

6 Dedication To everyone who has supported me through thick and thin v

7 Acknowledgements I would like to thank my supervisor, Dr. John McDonald, for welcoming me into the lab and providing a productive and inspiring environment to work in. Also, thank you for the wonderful guidance, ideas, feedback, and discussions that made this research possible. I would like to thank Greg Christie for the many discussions that contributed to this work and for his assistance with coding, trouble-shooting, analysis, and defense preparations. Thanks to John Gaspar and Ali Jannati for their assistance with equipment trouble-shooting. Also, thanks to Ashley Livingstone for her support and assistance with defense preparations. Thank you to Ulrich Anglas, T.J. Radonjic, Maksim Parfyonov, and Christina Hull for their help with data collection. I would also like to thank the staff in the Department of Psychology for all their assistance throughout the semesters. Finally, thank you to my family and friends who have encouraged me throughout the process. I am very grateful for the unwavering support of my husband Patrick who kept me focused on my goals and got me back on track when I veered off course. Also, I greatly appreciate the continuous support of Mom, Dad, Janelle, Stef, and Chris, even though they still don t fully understand what I do. Thank you! vi

8 Table of Contents Approval... ii Partial Copyright Licence...iii Abstract... iv Dedication... v Acknowledgements... vi Table of Contents...vii List of Tables... ix List of Figures... x 1. Introduction Early Studies of Covert Spatial Orienting in Audition Spatial Relevance Hypothesis Neuroimaging Recording Auditory Attention and ERPs Present Studies Experiment Methods Participants Apparatus Stimuli Design and Procedure Electrophysiological Recording Data Analysis Results and Discussion Behaviour Target-elicited ERPs Cue-elicited ERPs Experiment Methods Participants Apparatus Stimuli Design and Procedure Electrophysiological Recording Data Analysis Results and Discussion Behaviour Target-elicited ERPs Cue-elicited ERPs...34 vii

9 4. General Discussion References...43 viii

10 List of Tables Table 2-1. Inter-Participant Averages of Median Response Times (RT, in Milliseconds) and Standard Errors (SE) as a Function of Cue-Target Stimulus Onset Asynchrony (SOA) and Cue Type in Experiment Table 3-1. Inter-Participant Averages of Median Response Times (RT, in Milliseconds) and Standard Errors (SE) as a Function of Cue-Target Stimulus Onset Asynchrony (SOA) and Cue Type in Experiment Table 4-1. Summary of Behavioural and Electrophysiological Effects in the Spatial and Non-Spatial Tasks...39 ix

11 List of Figures Figure 2-1. Trial Sequences for Valid-Cue Trial (Left) and Invalid-Cue Trial (Right). These Illustrations are Examples of Go Trials Figure 2-2. Trial Sequences for a No-Go Trial (Left) and a Catch/No Target Trial (Right)...16 Figure 2-3. Grand-Averaged ERP Waveforms for Validly- and Invalidly-Cued Targets in Experiment Figure 2-4. Topographical Voltage Maps of the Nd and the Pd Elicited by Auditory Target Stimuli in Experiment Figure 2-5. Topographical Voltage Maps of Positive Deflections over Occipital Scalp in Experiment Figure 2-6. Grand-Averaged Event-Related Lateralization (ERLs) Elicited by Auditory Cues in Experiment 1. A. Ipsilateral and Contralateral Waveforms for T7/8 and PO7/8. B. Collapsed Ipsilateral and Contralateral Difference Waveforms for T7/8 and PO7/ Figure 2-7. Topographical Voltage Maps of the ACOP Elicited by Auditory Cue Stimuli...26 Figure 3-1. Grand-Averaged ERP Waveforms for Validly- and Invalidly-Cued Targets in Experiment Figure 3-2. Topographical Voltage Maps of the Nd Elicited by Auditory Target Stimuli in Experiment Figure 3-3. Topographical Voltage Maps of Positive Deflections over Occipital Scalp in Experiment Figure 3-4. Grand-Averaged Event-Related Lateralization (ERLs) Elicited by Auditory Cues in Experiment 2. A. Ipsilateral and Contralateral Waveforms for T7/8 and PO7/8. B. Collapsed Ipsilateral and Contralateral Difference Waveforms for T7/8 and PO7/ Figure 3-5. Topographical Voltage Maps of the ACOP in Experiment x

12 1. Introduction Everyone knows what attention is. It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. Focalization, concentration, of consciousness are of its essence. It implies withdrawal from some things in order to deal effectively with others, and is a condition which has a real opposite in the confused, dazed, scatterbrained state which in French is called distraction, and Zerstreutheit in German" (p ). ~ William James Every day, objects in the surrounding environment are competing for people s attention. For example, busy streets are lined with countless signs that are meant to attract the driver s attention and, if successful, their business. According to the attention and psychology literature, attention is the ability to attend selectively to relevant stimuli and ignore, or filter out, all irrelevant stimuli in the surrounding environment. A common example of this phenomenon is the cocktail party effect, where an individual is required to focus on a single person s voice and disregard all surrounding conversations and noise. This orienting of attention is important for extracting information from potentially important objects in the environment while avoiding distractions by less relevant objects. Although humans often direct their eyes and ears toward objects to which they attend, they can also direct their attention covertly, that is, without any corresponding eye or head movements. The latter is most often studied in research on spatial attention Early Studies of Covert Spatial Orienting in Audition In order to examine the attentional effects of covert auditory spatial attention, studies typically use a cueing paradigm, which involves an auditory cue that directs attention to the left or right of fixation, followed closely by an auditory target presented either in the same location as the cue (valid trial) or a different location as the cue (invalid trial). The cue can be predictive or non-predictive of the location of the target. Participants are generally faster and more accurate when responding to targets on valid 1

13 trials than invalid trials (Buchtel & Butter, 1988; McDonald & Ward, 1999; Posner, 1980; Quinlan & Bailey, 1995). Such cue effects have been largely interpreted in terms of the orienting of spatial attention. Specifically, participants are hypothesized to orient attention to the cued location prior to the onset of the target (Taylor & Klein, 1998). Spatial cueing studies have found that cues can have different effects on responses depending on the cue-target interval. If an auditory target is presented after a short time interval (within about 200 ms) and at the same location of an auditory cue, the response will be facilitated. This facilitation is considered to be under exogenous control since the observed cue effects are present even when the cues do not predict the location of the target. This control of attention is driven by a particular stimulus and is involuntary. However, if the cues predict the target location, the control of attention is said to be endogenous since the cues influence attention to shift voluntarily towards the correct target location, which in turn affects the response time to the target. This control of attention is goal-driven and voluntary (Posner & Cohen, 1984). Unlike the facilitation effect at short time intervals, if the cue-target duration is longer (about 700ms) the response to the target that appears at the same location as the cue is inhibited. This effect has been coined inhibition of return (IOR). IOR in an inhibitory component of covert orienting that hinders the ability to return attention to a location that had been just attended to and is measured by the delayed response to the later stimulus at the original cued location (Klein, 2000). Therefore, responses to valid trials are longer than to invalid trials. Although there is now general agreement that sudden sounds capture attention exogenously, there has been considerable debate about this in the past. Posner (1978) conducted several cueing studies in vision, audition, and touch and found that, unlike vision and touch, there were no spatial cueing effects for auditory targets when followed by informative central cues. This null effect occurred for both a simple detection task and target intensity discrimination go-no-go task. Buchtel and Butter (1988) reported that auditory or visual informative peripheral spatial cues did not affect latency detection for auditory targets but did affect detection of visual targets. Posner suggested the reason for the null effect is because auditory frequency detection occurs before sound localization. His rationale is that auditory receptors do not map spatial locations topographically, as they do in vision. The structural organization of the auditory pathway is designed to encode different sound frequencies along the structure. Therefore, he 2

14 suggested that sound location is determined by specialized, location-sensitive neurons thought to be in the colliculus (a structure in the midbrain that is involved in activating eye movements) or the auditory cortices. Buchtel and Butter (1988) took Posner s (1978) research further and investigated within- and between-modality spatial cueing effects using different combinations of visual and auditory cues and targets in a simple detection task. Cueing effects were elicited when visual cues (large cost-benefit effects) and auditory cues (small cost- benefit effects) preceded visual targets; however, when visual and auditory cues preceded auditory targets, no cueing effect was observed. This one-way influence was also found in other studies (e.g., Spence & Driver, 1997). Buchtel and Butter suggested covert spatial orienting occurs only when participants were required to respond to visual stimuli, because (1) overt movements of the eyes and head improve visual identification but not auditory identification (because the auditory system lacks an analog of the fovea), and (2) covert spatial orienting is linked to overt orienting systems. According to this proposal, covert orienting will occur in vision and touch but will not occur in audition, because accurate identification of sounds does not require spatial orienting. Rhodes (1987) revisited Posner s (1978) null effect by investigating the spatial properties of auditory attention. She claimed that covert spatial orienting would not be apparent in simple reaction time (detection) tasks since this task could be performed solely on the basis of non-spatial representations. Therefore, a localization task was used to ensure the use of spatial auditory representations, where participants responded verbally, using a previously learned label (e.g., 1, 2, 3, etc), to the location of the target sound. The locations of the sounds were spaced evenly around the participant and each had a number associated with it. Rhodes found that verbal response times increased linearly with the distance between the location of the target from a given trial and the location of the target from the preceding trial. This increase was argued to reflect the time attention took to shift between target locations at a constant rate. This explanation was adapted from vision research conducted by Tsal (1983), who provided evidence that it takes more time to shift attention across larger distances than shorter distances in the visual field. Although Rhodes results suggest that participants can orient attention covertly in auditory space, other researchers (e.g., Spence & Driver, 1994) have questioned whether the results reflect response priming rather than shifts of auditory attention. Specifically, Spence and Driver (1994) pointed out that because the semantic 3

15 distance between the learned labels also increased linearly as the distance between target sounds increased, participants simply might have counted up to the speakers that were numbered consecutively to get to the correct response. Following Rhodes (1987) lead to use spatial representation rather than simple detection to study covert spatial attention in audition, Spence and Driver (1994) used spatially predictive or non-predictive cues and cued participants in one direction (left or right) but required them to discriminate the target in an orthogonal direction (up or down). Therefore, participants discriminated the elevation of the target rather than its laterality. Spence and Driver found that participants were faster to respond to targets when the preceding cue was on the same side of the target as opposed to when the preceding cue was on the opposite side of the target. They also found that predictive spatial auditory cues elicited spatial orienting in both localization tasks as well as frequency discrimination tasks. The findings are consistent with the hypothesis from Rhodes that spatial orienting in audition will occur if the task requires auditory spatial representations but contradicts Buchtel and Butter s (1988) hypothesis that covert spatial orienting will never occur in audition because there is no sensitive receptor, such as a fovea. By using an orthogonal cueing paradigm, the cue effects cannot be explained in terms of response-priming by the cue. Amidst these general strengths of the orthogonalcueing task, there is one potential weakness: cues and targets never appear at the same location; and thus the orthogonal-cueing paradigm might underestimate the size of the attentional effects or miss attentional effects entirely because cues are always invalid to some degree (Prime, McDonald, Green, & Ward, 2008). Spence and Driver s (1997) explanation for this more rapid response to sameside cued targets is that less information is required to respond to ipsilateral cued targets than to contralateral cued targets. They reasoned that participants compared the location of the target with the location of the preceding cue. This comparison is much easier if the cue and target occurred on the same side. Another possible explanation is that there are different attentional neural mechanisms that are involved in the response to a target when the preceding cue is on the same side versus when the cue is on the other side of the target. Early research on visual attention suggested that attention is filtered from the receptive fields of specific neurons and only have enhanced processing when the cue and target were in the receptive field than when the cue was outside the receptive field (Moran & Desimone, 1985). Therefore, the location of the cue and target 4

16 has to be quite close in order for these mechanisms to activate. Yet another possible explanation for Spence and Driver s (1994) findings is that the attention effects (attentional facilitation and inhibition of return) are present only when the location of the cue and target are far apart, which has been hypothesized to be due to oculomotor preparation or suppression instead of activating receptive fields of specific neurons (Tassinari, Aglioti, Chelazzi, Marzi, & Berlucchi, 1987). Contrary to Rhodes (1987) claim that spatial representations need to be used in order to orient covert attention in audition, some studies have found that covert spatial orienting can occur in auditory detection and non-spatial discrimination tasks (Buchtel, Butter, & Ayvasik, 1996; Mondor & Zatorre, 1995; Mondor, Zatorre, & Terrio, 1998; Quinlan & Bailey, 1995; Roberts, Summerfield, & Hall, 2009). Quinlan and Bailey (1995) claimed that covert auditory attention effects occur at peripheral, non-spatial stages of the auditory system. Also, Mondor and Zatorre (1995) found that the time required to shift attention is independent of the distance of the shift, and therefore is not a linear increase as Rhodes found. Localization performance was dependent on the azimuthal (i.e., horizontal arc) location; however, these effects were not found for covert orienting of attention. This finding led the researchers to propose that auditory localization and auditory covert orienting depend on separate neural mechanisms, as well as auditory and visual covert orienting depend on different subcortical systems (inferior colliculus and superior colliculus, respectively; see also Buchtel, Butter, & Ayvasik, 1996, and Thompson & Masterton, 1978). There have been others (e.g., Farah, Wong, Monheit, & Morrow, 1989; Hillyard, Simpson, Woods, Van Voorhis, & Münte, 1984; Posner, 1987; Woods, 1990) who have speculated that the parietal lobe is involved in spatial attention in audition and in vision; however, the evidence for subcortical systems involved in auditory covert spatial orienting is incomplete. Another area in audition that is unclear is the spatial attentional effect of inhibition of return (IOR). Some studies have not found any evidence of an IOR in audition (Spence & Driver, 1994, 1997), while others only have found an IOR in audition when participants either prepared (Schmidt, 1996) or made overt (Reuter-Lorenz, Jha, & Rosenquist, 1996) eye movements to the cued location. These studies suggest that oculomotor programming is important in causing IOR in audition. This suggestion is found in several visual studies as well (Kingstone & Pratt, 1999; Posner & Cohen, 1984; Posner, Rafal, Choate, & Vaughan, 1985; Rafal, Calabresi, Brennan, & Sciolto, 1989). 5

17 However, still others have found an inhibitory effect in auditory attention (Facoetti et al., 2003; Mondor, Breau, & Milliken, 1998). This IOR has been found in different types of tasks, such as in location-based and frequency-based tasks (Mondor, Breau, & Milliken, 1998) as well as simple detection tasks (Tassinari & Berlucchi, 1995), without oculomotor preparation or execution. Therefore, it is unclear whether or not IOR is generated by the oculomotor system Spatial Relevance Hypothesis There have been some conflicting results regarding the necessary conditions for spatial covert orienting in audition to occur, as presented above. McDonald and Ward (1999) sought to clarify these contradictory results by introducing the spatial relevance hypothesis (SRH). The SRH revisits Rhodes (1987) claim that localization tasks are needed to ensure the use of auditory spatial representations to produce evidence for auditory covert spatial attention. More specifically, the SRH makes two main predictions about the spatial-orienting costs and benefits in auditory cueing tasks. The first prediction is that an auditory spatial cue effect will occur when space is relevant to the task, irrespective if the cue is predictive or non-predictive to the location of the target. The easiest way to make space relevant to the task is to use a spatial-discrimination task, although care should be taken to avoid the possibility of response priming by the cue. Such tasks require participants to localize sounds on the basis of spatial representations, which means that a spatial representation must be made available for spatial orienting to occur. This prediction is supported by several studies, when the cues are informative (Bédard, El Massioui, Pillon, & Nandrino, 1993; Quilan & Bailey, 1995; Spence & Driver, 1994) or uninformative (Quinlan & Bailey, 1995; Roberts et al., 2009; Spence & Driver, 1994, 1997; Ward, 1994; Ward, McDonald, & Lin, 2000) of the location of the target. The second prediction is that reflexive activation of location-sensitive auditory neurons is not sufficient to produce attentional facilitation or IOR (p.1236). Attentional facilitation or IOR depends on whether the task is spatially relevant. To test the SRH, McDonald and Ward (1999) conducted several spatial auditory attention experiments, using a modified spatial cueing paradigm. Their experiments consisted of different combinations of the spatial relevant and irrelevant tasks, as well as frequency discrimination tasks. For most of their experiments, cue and target tones were presented from either the centre speaker placed directly in front of the participant or 6

18 peripheral speakers placed to the right or left of the centre speaker. Depending on the experiment, participants were asked to respond to the peripheral targets and to withhold a response to the centre target (spatial go/no-go task) or to respond to high- and lowfrequency tones and withhold responses to middle-frequency tones (non-spatial go/nogo task). McDonald and Ward called the former task the implicit spatial discrimination task because, although participants were not asked to discriminate locations explicitly, processing of the spatial location was still necessary to perform the task well. Moreover, since the same response was required on valid and invalid trials, response priming was not a problem in the implicit spatial discrimination task. McDonald and Ward found that, at short SOAs, spatially uninformative auditory cues facilitated responses to auditory targets, whereas, at long SOAs, they inhibited the responses in the implicit spatial discrimination task. Critically, these effects were absent when the implicit spatial discrimination task was replaced by the analogous non-spatial task. This pattern of results spatial cue effects present in the spatial task but absent in the non-spatial task is consistent with the first prediction of the SRH. To provide further support for the SRH with respect to IOR, a final experiment was conducted, which used a target-target paradigm. Participants responded to each successive target and later responded to the spatially relevant targets. This experiment found that, even in the absence of cues, the spatial information of the previous target aided performance in the spatially relevant task but not when the task was spatially irrelevant. With the use of the implicit spatial discrimination paradigm, the cue effects observed in these experiments were not caused by response priming because space was made relevant to the participant s response without requiring participants to select a different response to different target locations from where the cue effects occurred. Therefore, McDonald and Ward (1999) concluded that participants activated locationsensitive neurons to perform the tasks, which in turn produced auditory covert spatial orienting effects. In regards to negative cueing effects, no speed-accuracy trade-off (i.e., more errors made on invalid trials than valid trials) was found in implicit spatial discrimination tasks (McDonald & Ward, 1999). The presence of IOR was found in spatial tasks but not in non-spatial tasks. When using identical cues in both types of tasks, it can be assumed that they would activate the oculomotor system equally. However, IOR occurred in the absence of oculomotor activation in spatial tasks, indicating that oculomotor preparation 7

19 or execution is not necessary for IOR to occur. These findings are inconsistent with the earlier claim that oculomotor activation is necessary to elicit IOR in audition (Reuter- Lorenz et al., 1996). Through their experiments, they found that spatial relevance is more important for a negative cueing effect (IOR) than oculomotor activity, which supports their second prediction. The SRH is similar to a theory found in visual studies. Folk, Remington, and Johnston (1992) were interested in investigating the conditions under which involuntary shifts of spatial attention occur. These researchers conducted a series of spatial and non-spatial visual experiments using a modified spatial cueing paradigm. Participants saw either a feature relevant cue (e.g., four dots) or a feature irrelevant cue (e.g., four red dots) that were non-predictive of the target ( + ) location. They found that the visual cue captured attention only when the uninformative cue matched (i.e., valid trial) the dimension that the observer was searching for; therefore, they found no involuntary orienting of attention in the non-spatial task. These researchers concluded that some visual spatial attentional processes are contingent on the task. There has been much support for this finding (Chen & Zelinsky, 2006; Folk, Leber, & Egeth, 2002; Folk, Remington, & Wright, 1994; Hommel, Pratt, Colzato, & Godijn, 2001; Most, Simons, Scholl, Jimenez, Clifford, & Chabris, 2001). This finding is similar to the SRH proposed by McDonald and Ward (1999) because it has the same conclusion as Folk et al. (1992). The spatial relevance hypothesis posits that for auditory covert spatial orienting to occur, the task must be spatially relevant to the task (i.e., auditory spatial processes are contingent on the task). However, these two hypotheses are in different modalities. The spatial orienting findings presented here are based on behavioural data. Even though non-spatial tasks did not result in a facilitatory or inhibitory effect in the behavioural data, studies on primates suggest that oculomotor activation occurs regardless of the task (Jay & Sparks, 1987a, 1987b). Also, the second prediction in the SRH states that reflexive activation of location-sensitive auditory neurons is not sufficient to produce attentional facilitation or IOR, (p. 1236; McDonald & Ward, 1999). This reflexive activation by the cues might have activated the oculomotor system equally in both the spatial and non-spatial tasks. Even though there were no attentional effects in the non-spatial tasks, investigating the neural mechanisms behind this equal activation might provide more information about the underlying processes involved in non-spatial tasks and also that are contingent on spatial tasks. 8

20 1.3. Neuroimaging Recording Researchers have used different neuroimaging techniques to examine the neural activity involved in spatial attention, focusing mostly on the visual modality. Hemodynamic methods, such as functional magnetic resonance imaging (fmri) and positron emission tomography (PET), provide information about metabolic activity and blood flow, respectively. These methods are generally used to produce high spatial resolution images of where the neural activity is occurring. In auditory spatial attention tasks, these techniques have localized neural activity in the frontal gyri in the prefrontal cortex, anterior cingulate cortex (ACC), middle cingulate cortex (MCC), superior parietal lobe (SPL), bilateral anterior insula, and bilateral putamen/caudate nuclei (Smith et al., 2010; Wu, Weisseman, Roberts, & Woldorff, 2007). A drawback to PET is its invasive nature since the participant has to ingest a radioisotope tracer in order for the scan to locate neural activation. Electrophysiological methods, such as electroencephalography (EEG), are used to record electrical neural activity associated with sensory, motor, and cognitive process. In a large group of pyramidal cells, simultaneous post-synaptic potentials summate and create large electrical fields that pass through the skull and scalp. The electrical fields are recorded non-invasively from the scalp during an experimental task. EEG has excellent temporal resolution of 1 ms or better, which is excellent since an action potential can take about ms (depending on the type of neuron) to travel down a single neuron, whereas PET and fmri are limited to a resolution of several seconds because of the slow tendency of the hemodynamic response (Luck, 2005). The excellent temporal resolution of EEG allows researchers to investigate the stages of information processing. With EEG, researchers are able to study the effect a cue has on a target stimulus, especially if they occur several 100 ms apart. In addition, this allows researchers to investigate the cue and target activity within the same stimulus range, which allows the comparison between different sets of cues and targets. Other neuroimaging techniques are not able to see these effects with their inferior temporal resolution. A disadvantage to using EEG methods is that it is unable to provide precise estimates of the locations of participating neurons. However, spatial distribution can be inferred from summations of large electrical fields that are recorded from several scalp electrode sites. A top-down approach can be utilized with certain software (e.g., BESA), which calculates the source that produced the electrical activity recorded at the scalp. 9

21 1.4. Auditory Attention and ERPs To investigate the neural correlates involved in auditory attention, epochs of EEG activity that are time-locked to a specific event are averaged together to create eventrelated potentials (ERPs). By averaging this activity from many trials, it reduces the activity that is not time or phase locked to the event of interest, which results in a waveform that represents the neural response of that specific event. The most common approach to investigate the effects of spatial attention processing is to compare ERPs elicited by the stimuli at attended locations and unattended locations. Several visual and auditory studies have found that when target (and non-target) stimuli are presented at attended locations, the elicited ERPs are more negative than when the stimuli appear at unattended locations. This negative difference (Nd) contains two phases (early and late), which suggests that there are multiple stages of processing when voluntarily shifting attention to a spatial location. The early Nd has been reported to begin as early as 60 ms and usually has a maximum deflection at the fronto-central electrode sites. Woldorff and colleagues (1993) suggested that the early Nd is generated in the auditory cortex on the supratemporal plane, just lateral to Heschl s gyrus. The early Nd is typically thought to reflect processing of low-level stimulus features (e.g., frequency), which helps to determine if the stimulus matches the target. In sustained-attention tasks, a subsequent negative difference called the late Nd typically occurs from approximately 250 ms to 500 ms post-stimulus. This waveform is thought to reflect the processing of the many features of the stimuli (Woods & Alain, 2001) and the maintenance of an attentional trace of the stimuli (Shelley et al., 1991). The amplitude of the late Nd is thought to represent the amount of attention allocated to the task (Gomes, Duff, Barnhardt, Barrett, & Ritter, 2007). The onset latency might reflect the duration of the processing required to determine the characteristics of the stimuli, and the peak latency might reflect time for processing to determine the significance of the stimulus (e.g., target) and the subsequent decision of the required action (e.g., button press) for that stimulus (Gomes et al., 2007). Most early ERP spatial attention experiments have focused on sustained attention paradigms, whereas Schröger and Eimer (1993) used a trial-by-trial paradigm where central cues were predictive of the target s location. They examined whether auditory spatial attention ERP effects in the trial-by-trial cueing paradigm are similar to 10

22 those found in a sustained attention paradigm. They found that the early Nd and late Nd onsets were around 125 ms and 200 ms, respectively. They called these two difference waves Nd1 and Nd2 (Schröger & Eimer, 1997). The Nd1 had a parietal scalp distribution, which contrasts the fronto-central distribution found in sustained attention for the early Nd. The scalp distribution for the Nd2 was fronto-central, which is slightly more posterior than the late Nd found in the sustained attention paradigm. This difference in scalp distribution indicated that sustained attention and transient spatial attention are generated by different neural processing. With most focus being on the visual modality, there have not been any ERP studies on exogenous cue effects in audition. Therefore, little is known about the neural mechanisms of these effects. However, there have been a few ERP studies on exogenous crossmodal attention effects, which provide some insight into the brain mechanisms involved in auditory spatial tasks and how these mechanisms might be linked. McDonald and Ward (2000) conducted a crossmodal experiment involving spatially non-predictive auditory cues and task-relevant visual targets. Participants were required to respond to peripheral targets by pressing a single button and to withhold responses to centrally presented targets that is, the standard implicit spatial discrimination task was used. McDonald and Ward found that participants responded faster to validly cued targets than to invalidly cued targets when the SOA was short (i.e., cueing benefit or attentional facilitation), with no difference for longer SOAs (i.e., no IOR effect). The voltage topographies showed two negative peaks during the shorter SOAs, with one over the contralateral occipital region and the other over the central region. This suggests that the Nd occurred in two different regions in the brain, with one in the modality-specific region, the visual cortex, and the other outside of the modality-specific region. These findings support the hypothesis that involuntary spatial attention orienting involves linked or shared brain mechanisms (McDonald & Ward, 1999; Spence & Driver, 1997). In another study, McDonald and colleagues provided further support for the hypothesis of linked or shared brain mechanisms (McDonald, Teder-Sälejärvi, Heraldez, & Hillyard, 2001). This time, spatially non-predictive visual cues were presented before task-relevant auditory targets. A modified implicit spatial discrimination task was used: participants were once again asked to withhold responses to centrally presented targets, but rather than making the same simple response to all peripheral targets, they were 11

23 asked to press different buttons depending on the frequency of the target sound. Behaviourally, participants were faster to respond on valid trials than on invalid trials. Electrophysiologically, the target ERPs were more negative on valid trials than invalid trials in the time ranges of the early Nd1 and later Nd2 components. They also found that the Nd occurred in two different regions of the brain, with the Nd1 peaking over parietal scalp ipsilateral to the target and the Nd2 peaking symmetrically over frontocentral scalp. These findings provide evidence that non-predictive visual cues aid participants to respond to nearby auditory targets and are consistent with the hypothesis that involuntary spatial attention orienting involves linked or shared brain mechanisms Present Studies The present experiments utilized intramodal auditory cueing paradigms and investigated the spatial cue effects on electrophysiological responses as well as behavioural responses, in both spatial and non-spatial tasks. By using electrophysiological recording methods, such as EEG, the neural mechanisms underlying the processes that are contingent on spatial tasks could be investigated. This will compliment the existing literature on auditory spatial attention that examined only behavioural effects (e.g., McDonald & Ward, 1999; Roberts et al., 2009). In Experiment 1, spatial relevance was established by requiring a spatial go/nogo response to the auditory targets. To do so, responses were made when the target occurred in the peripheral speakers but withheld to the targets presented in the centre speaker. This ensures that the target location is task relevant without having an explicit location-based discrimination task. Experiment 2 utilized the exact same cue and target tones as Experiment 1; however participants made non-spatial (frequency-based) go/nogo responses rather than spatial ones. These experiments were conducted with two primary goals. The first goal was to examine the behavioural attentional effects (i.e., attentional facilitation and IOR) in the first two experiments. By replicating the finding that attentional facilitation and IOR occur only in spatially relevant tasks, it can be certain that any neural activity time-locked to these effects is due to orienting of attention. The second goal was to compare the behavioural attentional effects with the target-elicited ERP waveforms, namely the Nd. The timing and topography of the Nd can help determine when, and what brain regions, 12

24 attention modulates auditory processing. If attentional effects are present when the task is spatially relevant, then corresponding neural activity would be expected in Experiment 1 but not in Experiment 2. Based on previous research (e.g., McDonald et al., 2001) and the spatial relevance hypothesis (McDonald & Ward, 1999), this hypothesis is expected. However, it might be the case that the behavioural data does not necessarily reflect attention processing. Therefore, if an Nd is also present in the non-spatial task, then this would indicate that non-predictive cues captured spatial attention even though it is irrelevant to the task. Because the orienting of attention is different in spatial and nonspatial tasks, it is possible that their scalp topographies would also be different. The presence of an Nd in a non-spatial task would be a novel finding. 13

25 2. Experiment 1 Experiment 1 is an auditory spatial task, where participants were asked to attend, and respond, to all tones from the peripheral speakers and to ignore the tones from the centre speaker Methods Participants Twenty healthy undergraduate students, between 18 and 32 years of age, from Simon Fraser University participated in this experiment. Data from one participant were excluded from the analyses as more than 30% of trials were rejected due to blink or eye movement artifacts. Of the remaining 19 participants (12 females, mean age = 22.9, 16 right-handed), all reported normal hearing and normal or corrected-to-normal vision. Written informed consent was received from all participants, as per the protocol of the ethics board at Simon Fraser University. The participants received course credit or payment for their participation Apparatus A sound-attenuated, electrically shielded chamber was used for the experiment. The chamber contained three speakers (Creative Inspire T speaker system) aligned horizontally in front of the participant. A Windows-based, Pentium-IV PC running Presentation (Neurobehavioral Systems Inc., Albany, CA, USA) presented the stimuli and recorded participants responses. Another Windows-based PC controlled EEG acquisition using Acquire (custom software). The acquisition PC was connected to a 64- channel analog-to-digital board (a 12-bit data-acquisition board; PCI-6071e; National Instrumentation, Austin, TX, USA), which was in turn connected to SA Instrumentation EEG amplifiers (SA Instrumentation Co., San Diego, CA, USA). 14

26 Stimuli Three target tones differing in frequency (1 khz, 1.73 khz, and 3 khz), with a duration of 50 ms and a rise and fall time of 5 ms, were used. The target tones were presented at 75 db, measured at the ears. The noise (cue) tone was a 70 ms noise burst (30 ms noise burst followed by a 10 ms blank interval followed by another 30 ms noise burst), with a rise and fall time of 5 ms. The cue tone was presented at 70 db, measured at the ears Design and Procedure The centre speaker was positioned directly in front of the participant, whereas the left and right speakers were positioned 38 to the left and right of the centre speaker, respectively. The speakers were raised to ear level. The participant sat in a dimly lit experimental chamber 57 cm from the centre speaker. To encourage participants to keep their eyes still, a fixation sticker measuring 1 cm x 1cm was placed in the centre of the centre speaker. Each trial began with a 70 ms noise-burst cue randomly from the left, centre, or right loudspeaker (40%, 20%, 40%, respectively). On most trials, a target was then presented to the left, centre, or right loudspeaker after a short silent interval. On 14% of trials, no target was presented. On the remaining trials, the cue-target stimulus-onset asynchrony (SOA) was either 150 ms (71% probability) or 900 ms (14% probability). Participants were instructed to press either a left or right button with their index finger on a gamepad when the onset of a target tone from the peripheral speakers (go trials) and asked to ignore target tones presented from the centre speaker (no-go trials). The response hand was randomly selected at the beginning of the experiment and then counterbalanced after the halfway point (i.e., after block 17) of the experiment. The cue was not predictive of the target's location. All tones were randomly presented from the speakers with a probability of 40% from the left, 20% from the centre, and 40% from the right speaker. The intertrial interval (ITI) was between 1,500 ms and 2,000 ms for all trials. Examples of the stimulus sequences on different trial types are displayed in Figures 2-1 and 2-2. At the end of three blocks, participants received verbal feedback on their performance from the experimenter. A mandatory 10-second rest break was taken after every block (about 1.5 minutes). Participants received a 5-minute break after 12 blocks (after about 18 minutes) where participants were able to play computer games or relax 15

27 Figure 2-1. Trial Sequences for Valid-Cue Trial (Left) and Invalid-Cue Trial (Right). These Illustrations are Examples of Go Trials. Figure 2-2. Trial Sequences for a No-Go Trial (Left) and a Catch/No Target Trial (Right). 16

28 their eyes. Data were collected in a single test session consisting of 35 blocks of 35 trials each block, resulting in 560 peripheral target trials (go trials), with 280 valid-cue trials and 280 invalid-cue trials Electrophysiological Recording EEG was recorded from 63 tin electrodes and was placed at FP1, FPz, FP2, AF3, AF4, F1, F3, F5, F7, Fz, F2, F4, F6, F8, FC1, FC3, FC5, FCz, FC2, FC4, FC6, C1, C3, C5, Cz, C2, C4, C6, T7, T8, CP1, CP3, CP5, CPz, CP2, CP4, CP6, P1, P3, P5, P7, Pz, P2, P4, P6, P8, PO3, PO7, POz, PO4, PO8, O1, Oz, O2, I3, I5, Iz, I4, I6, SI3, SIz, and SI4 (Electro-Cap International Inc.). Five electrodes were not positioned on the system; they were placed inferior to the occipital electrodes. The ground was placed on the midline between Cz and CPz. External electrodes were placed on both mastoids. All EEG signals were referenced to the right mastoid. Horizontal electrooculogram (HEOG) tracked eye movements using bipolar external electrodes that were placed 1 cm lateral to the right and left outer canthi. Blinks were monitored using the FP1 electrode. All impedances were kept below 10 kohms. All signals were amplified with a gain of 20,000, recorded with a bandpass of Hz (-3 db point; -12 db per octave) and digitized at 500 Hz using a SA Instrumentation amplifiers (a 12-bit data-acquisition board; PCI-6071e; National Instrumentation, Austin, TX, USA) and Acquire (custom Windows software). ERPSS (University of California, San Diego, CA, USA) was used to process the data offline. The data were epoched from 200 ms before target onset to 800 ms posttarget. All data were visually inspected offline for blinks, eye movements, and amplifier blocking and the trials containing these artifacts were excluded. Participants with excessive noise due to these artifacts were removed from further analysis. Trials that participants incorrectly responded to the centre speaker target were discarded. A digitally low-pass filter (-3 db cutoff at 25 Hz) was applied to remove high-frequency noise caused by muscle movements and external electrical sources. Averaged ERP waveforms were created from the artifact-free data Data Analysis Behavioural analysis. Trials with response times less than 100 ms, more than 1,500 ms, or with no response on a go trial were removed from further analysis. All tones 17

29 from the centre speaker were excluded from further analysis. Mean response times and false alarms were analysed in a 2 x 2 repeated-measures analysis of variance (ANOVA), with SOA (150 ms and 900ms) and Cue Type (valid and invalid) as the within-subject factors. Central (i.e., neutral ) cues were not included as a third level of the Cue Type factor because of the inherent difficulty of interpreting neutral" cues (cf. Jonides & Mack, 1984; Wright, Richard, & McDonald, 1995). Planned Bonferroni t-tests between valid-cue and invalid-cue conditions at both SOAs (two tests) were performed using the MSe from the experiment's SOA X Cue Type interaction to calculate the critical difference for the cue effects. These tests were two-tailed, with the familywise error rate set at ERP analysis. The difference waveforms were calculated by subtracting invalidcue trials from valid-cue trials. In order to remove overlapping cue ERPs and thus isolate the target-elicited ERPs for the short SOA, cue ERPs were averaged using the 900-ms SOA trials and no-target trials and were then subtracted from the target-elicited ERPs obtained on the 150-ms SOA trials. Target-elicited ERPs were collapsed across target location (left, right) and cue type (valid, invalid) to reveal ERP waveforms recorded contralateral and ipsilateral to the target location. For the analysis of the cue- and target-elicited waveforms, mean amplitudes were measured relative to a 100 ms pre-stimulus baseline. Separate t-tests were performed to compare the mean amplitudes of the target ERPs on valid and invalid trials in the time intervals of the N1 ( ms, at FCz), Nd ( ms, at FCz and PO7/8), and a subsequent positive difference (Pd) observed over the fronto-central scalp ( ms, at FCz). Three distinct positive deflections over occipital scalp ( ms) were analysed in a repeated-measures ANOVA, with Electrode as the sole withinsubject factor across the sites of interest. Planned comparisons were performed to compare the amplitudes of the sites of interest The mean voltages for the Nd and Pd amplitudes, as well as for a posterior positive deflection, were mapped for their latency ranges in order to estimate its neural generators. Voltage maps were used to visualize the distribution of the electrical fields across the scalp. To examine the topography of lateralized ERP activity, contralateralminus-ipsilateral voltage differences were calculated for homologous left and right electrodes (e.g., PO7 & PO8), the resulting voltage differences were assigned to electrodes on the right side of the head and were copied to electrodes on the left side of 18