Task analysis complements neuroimaging: an example from working memory research

www.elsevier.com/locate/ynimg NeuroImage 21 (2004) 1026 – 1036

Task analysis complements neuroimaging: an example from working memory research Daniel V. Meegan, * Rebecca Purc-Stephenson, Michael J.M. Honsberger, and Michael Topan Department of Psychology, University of Guelph, Guelph, Ontario, Canada N1G 2W1 Received 17 July 2003; revised 8 October 2003; accepted 8 October 2003

When functional neuroimaging researchers draw conclusions about the sensory, cognitive, or motor processes that are associated with changes in brain activity, they are making assumptions about the component processes involved in performing a complex behavioral task. We demonstrate the danger in making such assumptions using, as an example, the n-back task, which has been widely used in neuroimaging studies of working memory. Neuroimaging researchers have assumed that the letter n-back task only engages processes involved in the shortterm maintenance and manipulation of verbal information. We report three behavioral experiments demonstrating that the letter n-back task additionally recruits spatial processes. A fourth experiment suggested that the location n-back task may recruit verbal processes in addition to spatial processes. These results call into question conclusions that have been drawn about the neural basis of working memory. More broadly, our results demonstrate that task analysis is a vital partner of neuroimaging in the cognitive neuroscience enterprise. D 2003 Elsevier Inc. All rights reserved. Keywords: n-back task; Working memory; Functional neuroimaging; Premotor cortex; Posterior parietal cortex; Spatial; Verbal; Executive

Introduction Recently developed functional neuroimaging methodologies, such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET), have made important contributions to the understanding of the neural basis of sensory, cognitive, and motor behavior. The scope of these contributions is limited, however, for a variety of reasons (D’Esposito et al., 1999; Friston et al., 1996; Jennings et al., 1997; Kosslyn, 1999; Newman et al., 2001; Poeppel, 1996; Uttal, 2001). One critical limitation of neuroimaging is that it requires that assumptions are made about the component processes involved in performing a behavioral task. When a neuroimaging report states that a change in activity in a particular brain region (or regions), measured while participants perform a task, is associated with a particular process, the authors have assumed that (a) the process is required for performance of the task, and (b) no other processes required for performance of the task are associated with the change in activity. Long before * Corresponding author. Fax: +1-519-837-8629. E-mail address: [email protected] (D.V. Meegan). Available online on ScienceDirect (www.sciencedirect.com.) 1053-8119/$ - see front matter D 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2003.10.011

neuroimaging tools were developed, cognitive psychologists had developed methods for determining the component processes comprising cognitive tasks. Thus, it is critical that cognitive psychology be used in conjunction with neuroimaging to confirm which processes are involved in which tasks. Although in some cases neuroimaging researchers directly adopt tasks for which cognitive psychology has thoroughly analyzed the component processes, this is not always the case. An example of the latter is the n-back task (Cohen et al., 1994; Gevins et al., 1990), which has been widely used in neuroimaging studies of working memory despite minimal prior task analysis.1 In the nback task, participants are presented with a sequence of stimuli, and asked to judge whether the current stimulus matches the stimulus that preceded it by n places in the sequence. For example, in a 3-back task with the sequence of letters B, Q, D, P, Q, participants should respond positively to the second Q because it matches the letter that appeared three letters earlier. Neuroimaging researchers were attracted to the n-back task for several reasons (Braver et al., 1997; Cohen et al., 1997; Jonides et al., 1997). First, the n-back task was thought to be a more representative example of a working memory task than the tasks used in earlier neuroimaging studies because it was presumed to require manipulation of information held in working memory in addition to mere maintenance of information. Second, it allowed the use of the method of parametric variation instead of the method of subtraction, thereby avoiding some of the problematic assumptions associated with the latter (Friston et al., 1996; Jennings et al., 1997). Third, manipulation of the value of n allowed the systematic manipulation of working memory load, and brain regions showing changes in activity coincident with changes in load were thought to play specific processing roles. Neuroimaging researchers have rationalized their use of the n-back task, despite a lack of task analysis, by claiming that it activates the same brain areas as other working memory tasks whose component processes are well understood. There are at least two consistent exceptions to this claim: dorsolateral Brodmann area 6 (dorsal premotor cortex, or PMd) and right posterior parietal cortex (PPC), two regions that are not active during other nonspatial working memory tasks, are active during nonspatial n-back tasks (D’Esposito et al., 1998; Smith and Jonides, 1999). 1 The n-back task is so commonly used in neuroimaging research that it is impractical to cite every study that has been published to date.

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According to current theory, which was introduced by Baddeley and Hitch (1974) and refined by many contributors (Baddeley, 1986; Baddeley and Logie, 1999), there are two main types of component systems involved in working memory tasks: the executive system and the subordinate systems. The executive controls the maintenance, manipulation, and retrieval of the contents of working memory, and is thought to be involved in all working memory tasks regardless of the domain of information that is being maintained. Different subordinate systems, under the control of the executive, are thought to be involved in the maintenance of specific domains of information (e.g., verbal, spatial, and visual form). In other words, the executive is thought to be a domain-general system, whereas the subordinate systems are thought to be domain-specific systems. Neuroimaging studies of working memory have exploited this distinction in an effort to identify the brain regions associated with these systems. The logic is as follows: if you design two working memory tasks that are identical except for the domain of the information to be maintained, then brain regions that are activated by both tasks (excepting sensory and motor activation) are associated with the executive, and brain regions that are activated by just one of the tasks are associated with one of the subordinate systems. Studies employing this logic have concluded that prefrontal cortical areas are associated with the executive, and more posterior regions, especially in parietal and frontal cortices, are associated with the different subordinate systems (D’Esposito et al., 1998; Smith and Jonides, 1999). Before the n-back task was introduced in neuroimaging studies, regions of activity in PMd and right PPC were associated with the spatial subordinate system (Jonides et al., 1993). However, studies using the n-back task have shown that PMd and right PPC are active for all domains of information, not just spatial information (e.g., D’Esposito et al., 1998; Nystrom et al., 2000; Postle et al., 2000b; Zurowski et al., 2002). Application of the aforementioned logic forces the conclusion that these PMd and right PPC activations are associated with domain-general processes rather than spatial-specific processes. An alternative possibility is that erroneous assumptions have been made about the component processes involved in the n-back task. The n-back task is similar to other working memory tasks in that it requires the maintenance of stimulus identity and serial position information. However, the n-back task is unique in that it requires the dynamic comparison of serially presented stimuli. Perhaps such comparisons are aided by the mental transformation of serially presented information into a spatial representation. Experiments 1, 2, and 3 were designed to test the hypothesis that the n-back task, regardless of the domain of information to be maintained, recruits spatial processing.

Experiment 1 Participants performed a letter n-back task, and responded verbally in one condition and spatially in another. According to the existing literature, the letter n-back task is purely reliant on the executive and the verbal subordinate system. This view predicted that memory performance should be susceptible to disruption from verbal responding, but not spatial responding (Baddeley, 1986; Brooks, 1968). Our hypothesis suggests that the letter n-back task additionally recruits the spatial subordinate system. Thus, we predicted that memory performance should also be susceptible to disruption from spatial responding.

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For both verbal and spatial responding, there was a control condition and an experimental condition. In the control conditions, subjects made a single response to indicate whether the current letter was a match, and in the experimental conditions, subjects continued responding until the next letter appeared. Both the control and experimental conditions recruited executive processes required for comparing the current letter to the n-back letter, making a match decision, and making a differentiated response according to the decision. Forcing participants to continue responding in the experimental conditions was designed to disrupt the subordinate system(s) required for maintaining information necessary for subsequent trials. Materials and methods Participants Twenty-nine participants volunteered in return for credit toward a psychology course requirement. Participants were right-handed, had normal or corrected-to-normal vision, and were native speakers of English. The study received ethical approval from the University Human Subjects Committee of the University of Guelph, and all participants gave their informed consent before their inclusion in the study. Apparatus The experiment was controlled on a personal computer using E-Prime (Psychology Software Tools, Pittsburgh, PA). Participants’ responses were registered with a PST Serial Response Box (Psychology Software Tools) interfaced to the computer. Vocal responses were made into a microphone connected to the Serial Response Box. Manual responses were made onto a unit designed with the Custom Expansion Kit (Psychology Software Tools) and interfaced to the Serial Response Box. The manual response unit contained four buttons arranged in a rectangle, with 23 cm separating the buttons in diagonally opposite corners. Design and procedure Participants performed 1-back and 3-back tasks in separate sessions on consecutive days. During each session, there were four blocks of 60 trials, with one block for each of four response conditions. In each block, participants were presented visually with a sequence of 60 letters, chosen from a set of 18 letters. Vowels, and the consonants L, W, and Y were excluded from the letter set to minimize the pronounceability of strings of consecutive letters (Nystrom et al., 2000). Letters were presented in either upper or lower case, determined randomly, to encourage verbal, instead of visual, coding of the letters (Nystrom et al., 2000). Each block contained 20 matches (1-back matches in the 1-back task and 3-back matches in the 3-back task) and 40 nonmatches. Of the 40 nonmatches in each block, eight were foils that matched a nearby letter in the sequence: four 2-back matches and four 3-back matches occurred in the 1-back task, and four 1back matches and four 2-back matches occurred in the 3-back task (Jonides et al., 1997). Because the first three letters in any block of the 3-back task were guaranteed nonmatches, the first three responses in both the 3-back and 1-back task were not included in the analysis. Stimulus duration was 500 ms and the interstimulus interval (ISI) was 2500 ms. Each letter appeared in the center of a CRT display, as did a fixation cross that was present during the ISI.

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Four response conditions governed how participants were to indicate whether the current letter was a match or a nonmatch. In the verbal control condition, participants were to say ‘‘yes’’ once to indicate a match, or ‘‘no’’ once to indicate a nonmatch. In the verbal repeated condition, participants were to say ‘‘yes’’ repeatedly to indicate a match, or ‘‘no’’ repeatedly to indicate a nonmatch. In both verbal conditions, the identity of the response was entered into the computer by the experimenter, and, in the verbal repeated condition, the experimenter also entered the response frequency. In the spatial control and spatial repeated conditions, participants responded manually on the response unit with the hands covered from view. In both spatial conditions, before each letter presentation, the right hand was near the lower right button, and the left hand was near the lower left button. In the spatial control condition, the participants were to press the lower right button once with the right hand to indicate a match, or the lower left button once with the left hand to indicate a nonmatch. In the spatial repeated condition, on matching trials, participants were to consecutively press the lower right button and upper left button repeatedly with the right hand, or, on nonmatching trials, participants were to consecutively press the lower left button and upper right button repeatedly with the left hand. Response identity and response frequency were recorded automatically via an interface between the manual response unit and the computer that controlled stimulus presentation. Reaction time was also measured at the first response following each letter presentation in all response conditions (using a voice key in the verbal conditions). On all trials, an auditory warning signal occurred 500 ms before the onset of the next letter. The frequency of the auditory signal provided feedback concerning the accuracy of the preceding response. In the repeated conditions, participants were instructed to stop responding upon hearing the signal. In the spatial repeated condition, participants were to return the right hand to the lower right button or the left hand to the lower left button at this time. Results The design was a 2 (1-back, 3-back)  2 (verbal, spatial)  2 (control, repeated) repeated-measures ANOVA with accuracy as the dependent variable. If the letter n-back task recruits the verbal subordinate system, then the verbal repeated condition should have lower accuracy than the verbal control condition, and if the letter nback task recruits the spatial subordinate system, then the spatial repeated condition should have lower accuracy than the spatial control condition. The existing literature, which viewed the letter n-back task as a purely verbal task, expected a main effect of the verbal/spatial factor (with lower accuracy in the verbal than spatial conditions), and/or an interaction of the verbal/spatial and control/ repeated factors (with a negative effect of repetition in the verbal conditions and a zero effect of repetition in the spatial conditions). Our hypothesis, which viewed the letter n-back task as a verbal and spatial task, expected a main effect of the control/repeated factor (with a negative effect of repetition in both verbal and spatial conditions), and/or an interaction of the verbal/spatial and control/ repeated factors (with the negative effect of repetition differing in magnitude between the verbal and spatial conditions). The results are displayed in Fig. 1. As expected by our hypothesis, there was a main effect of the control/repeated factor [ F(1,28) = 43.82, P < 0.001], with lower accuracy in both the

Fig. 1. Mean percentage of correct (and standard error) on letter 1-back and 3-back decisions as a function of response condition in Experiment 1.

verbal and spatial repeated conditions relative to their respective controls. A main effect of the 1-back/3-back factor [ F(1,28) = 295.05, P < 0.001], with lower accuracy in the 3-back task than in the 1-back task, was expected because of the increased memory load in the former (Nystrom et al., 2000). No other effects were significant. In other words, the results suggested that the letter n-back task requires both verbal and spatial processing. Although accuracy was the dependent measure of interest, response time was also analyzed to confirm that a speed – accuracy tradeoff did not influence the accuracy results. The only significant effect was a main effect of the 1-back/3-back factor [ F(1,28) = 38.37, P < 0.001], with higher response time in the 3-back task than in the 1-back task (Nystrom et al., 2000), which was consistent with the fact that accuracy was lower in the former. The pattern of accuracy data could not be attributed to adjustments in speed. Another variable that could have affected the accuracy data was the response frequency in the repeated conditions. We did not expect that participants would respond with equal frequency in the verbal and spatial repeated conditions, as they are two very different responses. We deliberately avoided controlling frequency because we were concerned that maintaining a particular frequency may have been more difficult in one condition than in the other, thereby affecting the results in an unwanted manner. Mean response frequency was higher [t(28) = 6.65, P < 0.001] in the verbal repeated condition (6.1 responses per trial) than in the spatial repeated condition (4.0 responses per trial) for the 1-back task. For the 3-back task, mean response frequency was also higher [t(28) = 7.40, P < 0.001] in the verbal repeated condition (5.7 responses per trial) than in the spatial repeated condition (3.6 responses per trial). Although this quantitative comparison does not explain the poor performance in the spatial repeated condition, it is more important to know whether participants adopted qualitatively similar frequencies for each condition. This was accomplished by calculating the correlation between response frequency and memory error (difference score between control and repeated conditions) for verbal and spatial conditions. This correlation was significant for neither verbal (r = 0.16, P > 0.10) nor spatial (r = 0.04, P > 0.10) conditions in the 1-back task, and neither verbal (r = 0.28, P > 0.10) nor spatial (r = 0.13, P > 0.10) conditions in the 3-back task. In other words, the response frequencies adopted by participants in

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the spatial and verbal conditions had similar impacts on memory performance.

Experiment 2 The fact that the spatial and verbal response tasks were equally disruptive to letter n-back performance in Experiment 1 could be attributed to the possibility that the spatial task was generally more difficult. Thus, it was important to assess the relative impact of the verbal and spatial response tasks on another letter working memory task thought to recruit the verbal subordinate system, but not the spatial subordinate system. Participants were presented with sequences of eight letters, and asked to recall the letters immediately following the presentation of the eighth letter. During the intervals between letters, participants were required to perform one of two secondary tasks modeled after the verbal repeated and spatial repeated conditions used in Experiment 1. We predicted that the verbal secondary task would be more disruptive than the spatial secondary task, because the former would engage the rehearsal component of the verbal subordinate system. Materials and methods Participants Thirty-two participants volunteered in return for credit toward a psychology course requirement. Participants were right-handed, had normal or corrected-to-normal vision, and were native speakers of English. The study received ethical approval from the University Human Subjects Committee of the University of Guelph, and all participants gave their informed consent before their inclusion in the study. Apparatus The apparatus was the same as was used in Experiment 1. Design and procedure On each trial, participants were shown a visual sequence of eight letters drawn randomly without replacement from the letter set used

Fig. 3. Recall accuracy as a function of serial position and secondary task condition in Experiment 2. Error bars represent the 95% confidence intervals.

in Experiment 1. Following the last letter, they attempted to vocally recall the letters in any order. The experimenter identified their responses by pressing the corresponding keys on the computer keyboard. The duration, appearance, and position of stimuli, and the ISI between letters, were the same as in Experiment 1. During each ISI, until an auditory warning signal that occurred 500 ms before the onset of the next letter, participants were required to perform one of two secondary tasks modeled after the verbal repeated and spatial repeated conditions used in Experiment 1. In the verbal condition, participants were to say ‘‘yes’’ repeatedly, and in the spatial condition, participants were to consecutively press the lower right button and upper left button of the response unit repeatedly with the right hand. Participants performed one 20-trial block for each condition in counterbalanced order. Results

Fig. 2. Mean percentage of correct (and standard error) for letter recall as a function of secondary task condition in Experiment 2.

Recall accuracy in the verbal and spatial conditions was compared. The results are presented in Fig. 2. As expected, participants recalled fewer letters in the verbal condition than in the spatial condition [t(31) = 7.36, P < 0.001]. In other words, letter immediate recall performance was affected more by the verbal response task than the spatial response task. It is also noteworthy that recall accuracy was quite poor. This suggests that it would be difficult to argue that the presence of spatial interference in Experiment 1 and the absence of spatial interference in Experiment 2 was the result of the relative ease of the memory task used in the latter. Serial position curves for the spatial and verbal conditions are presented in Fig. 3. A 2 (verbal, spatial)  8 (serial positions 1 – 8) repeated-measures ANOVA revealed main effects of secondary task condition [ F(1,31) = 53.90, P < 0.001] and serial position [ F(7,25) = 10.38, P < 0.001], as well as an interaction [ F(7,25) = 2.76, P < 0.05]. Simple-effects analyses examined the effect of

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serial position for each secondary task condition separately. Serial position had a significant effect in both the spatial [ F(7,25) = 5.82, P < 0.001] and verbal [ F(7,25) = 8.57, P < 0.001] conditions. The 95% confidence intervals are represented in Fig. 3. A primacy effect occurred in the spatial condition, presumably because the first two letters were rehearsed more thoroughly than the last six letters. The absence of a recency effect, and the high recall accuracy for letters in the middle serial positions, indicates that the spatial secondary task was not at all disruptive. In the verbal condition, recall accuracy for letters in the middle serial positions was affected, demonstrating the disruptiveness of the verbal secondary task. Note also that existence of a recency effect under verbal secondary task conditions is consistent with working memory theory (Baddeley, 1986). It was also important to determine whether the response frequencies adopted by participants influenced accuracy. As in Experiment 1, mean response frequency was higher [t(31) = 15.30, P < 0.001] in the verbal condition (17.4 responses per trial) than in the spatial condition (8.99 responses per trial). The correlation between response frequency and accuracy was significant for neither the verbal condition (r = 0.04, P > 0.10) nor the spatial condition (r = 0.26, P > 0.10), suggesting that the response frequencies adopted by participants in the verbal and spatial conditions had similar impacts on memory performance.

approval from the University Human Subjects Committee of the University of Guelph. All participants gave their informed consent before their inclusion in the study, and received $5 as compensation for their time. Participants were right-handed, had normal or corrected-to-normal vision, and were native speakers of English. Participants were made aware that their eyes would be tracked during the study, although they were naı¨ve to our hypothesis that the eyes would behave differently in different tasks. Apparatus The software that controlled the experiment was developed in Matlab (MathWorks, Natick, MA) using the Psychophysics Toolbox (Brainard, 1997; Pelli, 1997) and the Data Acquisition Toolbox (MathWorks). The stimuli were displayed on a 19-in. monitor at 1024 (horizontal)  768 (vertical) resolution, and manual responses were made on a keyboard. The computer system was interfaced to an ASL 5000 series eye tracking system (Applied Science Laboratories, Bedford, MA), which employs the pupil/ corneal reflection technique for determining eye position. The eyes were tracked using a remote video camera equipped with pan-tilt optics that can follow the eyes in the event of minor head movements. Gaze position and pupil size were sampled at 60 Hz. A chin rest restricted head movements and maintained a viewing distance of 68 cm. The visual angle subtended by the letter stimuli varied from 1.07j (‘‘r’’) to 2.14j (‘‘M’’).

Experiment 3 Eye movements during spatial cognitive tasks are considered to be an external manifestation of internal spatial processing (e.g., Brandt and Stark, 1997; Hebb, 1968; Laeng and Teodorescu, 2002). Monitoring gaze position is particularly effective at gauging spatial processing when the spatial nature of the task is not obvious (e.g., Kennedy and Murray, 1987; Richardson and Spivey, 2000; Spivey and Geng, 2001). For example, Richardson and Spivey (2000) reported that participants tended to return the eyes to the spatial source of recently presented information even though the spatial information was irrelevant for performing the task. Because the spatial nature of the letter n-back task is perhaps even less obvious, as the letters are typically presented at the same location, we thought it would be informative to monitor gaze position while participants performed a letter n-back task. As in Experiment 1, all letters were presented at the same central location; thus, eye movements to locations outside of the central area would provide valuable information concerning the spatial nature of the task. An interesting characteristic of the PMd and right PPC activity associated with n-back performance is that it is load-dependent; in other words, as the value of n increases, the amount of activity measured in PMd and right PPC increases (Cohen et al., 1997; Jonides et al., 1997). We tested the possibility that increasing the value of n from one to three would produce a corresponding increase in oculomotor activity. Such load-dependent eye activity would be consistent with our suggestion that the letter n-back task is a spatial task. Materials and methods Participants Twenty-eight volunteers from the University of Guelph community participated in this study. The study received ethical

Design and procedure Participants first underwent a calibration procedure that confirmed accurate gaze coordinates for nine points on the stimulus display. There were two blocks of each task (i.e., 1-back and 3back), done in counterbalanced order, with the first being a practice block. In each block, participants were presented visually with a sequence of 45 letters, chosen from the set of 18 letters used in Experiments 1 and 2. Each block contained 15 matches and 30 nonmatches. Of the 30 nonmatches in each block, five were foils that matched a nearby letter in the sequence. Participants were to indicate a match by pressing the ‘‘Z’’ key (marked with green tape) once with the left hand, or a nonmatch by pressing the ‘‘/’’ key (marked with red tape) once with the right hand. No warning or feedback signals were provided. The procedure was otherwise identical to that used in Experiment 1. Data analysis The horizontal and vertical components of gaze position, and pupil size, were sampled continuously at 60 Hz from the beginning to the end of each block. Gaze coordinates were transformed from ASL coordinates (261  240) to display coordinates (1024  768) using a transformation adapted from that used by Duchowski et al. (2000). Samples with a pupil size of zero (indicating a blink), or a gaze position outside of the display, were filtered. Saccades were analyzed using ILAB (Gitelman, 2002). During testing, we became concerned that several of the participants were not sufficiently motivated to perform the difficult 3-back task as instructed. To ensure that the analysis only included participants who were attempting to do the task as instructed, we established a criterion of 60% correct on foil trials in the 3-back task. Foil trials are an excellent way of determining whether a participant is performing the task as instructed, because an obvious ‘‘lazy’’ strategy is to respond positively to any recently seen letter regardless of whether it was a 1-back, 2-back, or 3-back match. Six

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subjects failed to meet the criterion, and their data were not included in the analysis.

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Note that both tasks showed an upward and rightward bias, which was larger in the 3-back task.

Results Experiment 4 As in Experiment 1, participants were more accurate [t(21) = 6.87, P < 0.001] in the 1-back task (mean = 95.87% correct) than in the 3-back task (mean = 83.08%), and were faster [t(21) = 6.88, P < 0.001] to respond on correct trials in the 1-back task (mean = 656 ms) than in the 3-back task (mean = 1019 ms). Consistent with previous reports demonstrating that pupil size and task difficulty are positively related (Beatty, 1982), pupil size was larger [t(21) = 4.63, P < 0.001] during the 3-back task (mean = 7.02 mm) than the 1-back task [mean = 6.66 mm]. We hypothesized that increasing the value of n from one to three would produce a corresponding increase in eye movements. To test this hypothesis, we compared the 1-back and 3-back tasks in terms of (a) saccade frequency, and (b) the variability (i.e., standard deviation) of the horizontal and vertical components of gaze position. As expected, participants made more [t(21) = 3.13, P < 0.01] saccades in the 3-back task (mean = 109 saccades) than they did in the 1-back task (mean = 75 saccades). The variability data are represented in Fig. 4. Consistent with our hypothesis, horizontal variability was higher [t(21) = 3.56, P < 0.005] in the 3back task (mean = 39.73 pixels) than in the 1-back task (mean = 28.12 pixels), and vertical variability was higher [t(21) = 2.56, P < 0.05] in the 3-back task (mean = 50.84 pixels) than in the 1-back task (mean = 42.65 pixels). Neither the mean horizontal position [t(21) = 1.36, P > 0.10] nor the mean vertical position [t(21) = .32, p > 0.10] were different for the 3-back and 1-back tasks, indicating that the variability occurred relative to the letter position. Fig. 4 represents the standard deviations of gaze position for the 1-back and 3-back tasks, and the position of the center of the letter stimuli.

When discussing possible explanations for why letter and location n-back tasks, relative to other verbal and spatial working memory tasks, do not show as much differential brain activation in neuroimaging studies, Fiez (2001) considered two possibilities.2 First, the letter n-back task does not rely on the verbal subordinate system. This possibility was ruled out by Experiment 1, which demonstrated significant disruption of letter n-back performance by concurrent verbal responding (see also Awh et al., 1996). The second possibility considered by Fiez (2001) was that the location n-back task relies on the verbal subordinate system. Experiment 4 was designed to test this possibility, by having participants perform a location n-back task under concurrent verbal and spatial response conditions. Materials and methods Participants Thirty-two participants volunteered in return for credit toward a psychology course requirement. Participants were right-handed, had normal or corrected-to-normal vision, and were native speakers of English. The study received ethical approval from the University Human Subjects Committee of the University of Guelph, and all participants gave their informed consent before their inclusion in the study. Apparatus The apparatus was the same as was used in Experiments 1 and 2. Design and procedure Participants performed a location 3-back task in four blocks of 60 trials, with one block for each of four response conditions. The four response conditions were identical to those used in Experiment 1. In each block, participants were presented visually with a sequence of 60 circles, with the location of each circle chosen from a set of 16 locations equidistant from the center of the display. The task of the participant was to determine whether the current stimulus appeared at the same location as the 3-back stimulus. The procedure was otherwise identical to the 3-back task used in Experiment 1. Results The design was a 2 (verbal, spatial)  2 (control, repeated) repeated-measures ANOVA with accuracy as the dependent variable. If the location n-back task is more reliant on spatial than verbal processing, then there should be a main effect of the verbal/ spatial factor, and/or an interaction. If the location n-back task recruits the spatial subordinate system, then the spatial repeated condition should have lower accuracy than the spatial control condition, and if it recruits the verbal subordinate system, then

Fig. 4. Variability of gaze position as a function of n in Experiment 3. The ellipses were drawn using the horizontal and vertical means of gaze position plus/minus the standard deviations. The cross represents the center of the letter stimuli.

2

Fiez (2001) did not consider a third possibility: the letter n-back task relies on the spatial subordinate system. This third possibility was supported by the results of Experiments 1, 2, and 3 of the current paper.

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the verbal repeated condition should have lower accuracy than the verbal control condition. The results are displayed in Fig. 5. There was a main effect of the verbal/spatial factor [ F(1,31) = 27.67, P < 0.001], with lower accuracy in the spatial compared to the verbal conditions. In other words, spatial responding was more disruptive to location n-back performance than verbal responding. There was also a main effect of the control/repeated factor [ F(1,31) = 44.79, P < 0.001], with lower accuracy in the repeated conditions relative to the control conditions. The finding that the verbal repeated condition produced more interference than the verbal control condition [t(31) = 4.20, P < 0.001] is consistent with Fiez’s (2001) suggestion that the location n-back task may recruit verbal processing. Although it appeared (see Fig. 5) that the difference between spatial repeated and spatial control [t(31) = 5.52, P < 0.001] was greater than the difference between verbal repeated and verbal control, the interaction of the verbal/spatial and control/repeated factors failed to reach significance [ F(1,31) = 3.14, P = 0.086]. In summary, although spatial responding was more disruptive to location nback performance than verbal responding, there was also an impact of verbal repeated responding. In the response time analysis, the only significant effect was a main effect of the verbal/spatial factor [ F(1,31) = 6.80, P < 0.05], with higher response time in the spatial compared to the verbal conditions. This provided further confirmation that the location nback task relies more heavily on spatial than verbal processes. Although one might assume that this effect could simply be due to the verbal response being faster than the spatial response (under any task conditions), this was not the case when the same responses were used in Experiment 1. As in Experiments 1 and 2, we analyzed response frequency in the repeated conditions. Mean response frequency was higher [t(31) = 4.78, P < 0.001] in the verbal condition (5.7 responses per trial) than in the spatial condition (4.1 response per trial). Importantly, the correlation between response frequency and accuracy was significant for neither the verbal condition (r = 0.09, P > 0.10) nor the spatial condition (r = 0.10, P > 0.10),

Fig. 5. Mean percentage of correct (and standard error) on location 3-back decisions as a function of response condition in Experiment 4.

suggesting that the response frequencies adopted by participants in the verbal and spatial conditions had similar impacts on memory performance.

Discussion Spatial processing in the letter n-back task Experiment 1 demonstrated that spatial responding was as disruptive as verbal responding to letter n-back performance. Experiment 2 demonstrated that spatial responding was less disruptive than verbal responding to letter-immediate-recall performance. Experiment 3 monitored the eyes during letter n-back performance, and showed that saccade frequency and the spatial variability of gaze position were load-dependent. Taken together, these results suggest that the letter n-back task, unlike other letter working memory tasks, recruits spatial processing. The n-back task seems more dependent than the immediate recall task on processes associated with the executive system. If this is true, then it seems unclear whether the disruption of n-back performance by spatial responding in Experiment 1 was due to the executive requirements of the spatial response task, or, as we suggest, to the spatial requirements of the task. To address this issue, we compared the repeated task to a control task designed to be comparably disruptive of the executive aspects of n-back performance. Nevertheless, one could argue that there are other executive aspects of n-back performance that would be more susceptible to disruption from the repeated task than the control task. For example, after an n-back decision is made and the participant makes a single response, the contents of memory might need updating and reorganizing, and continued responding might disrupt these executive processes. This issue was addressed by Awh et al. (1996) who demonstrated that nonspatial manual repeated responding did not disrupt letter n-back performance. Given that the spatial manual responding used in the current study and the nonspatial manual responding used by Awh et al. (1996) had similar executive requirements, and differed primarily in their spatial requirements, we suggest that the disruption we found in Experiment 1 was due to the spatial requirements of the spatial repeated condition. One might argue, though, that there is a nonspatial process that distinguishes between the spatial repeated task used in Experiment 1 and the response task used in Awh et al. (1996). More specifically, the spatial repeated task used in Experiment 1 required response alternation (between a response to one corner and a response to the opposite corner), whereas the task used in Awh et al. (1996), and the verbal repeated task used in Experiment 1, did not require alternation. In other words, the results of Experiment 1 cannot rule out the possibility that the disruption of letter n-back performance by manual repeated responding was due to a process related to response alternation, rather than a spatial process. However, there are several studies that have demonstrated that response alternation (excepting vocal responses) does not disrupt executively demanding verbal working memory tasks (e.g., Baddeley and Lieberman, 1980; Baddeley et al., 1975; Brooks, 1968; Quinn, 1988, 1991; although, see Troyer et al., 1997). For example, Brooks (1968) used a verbal task in which participants were to keep a 10-word sentence in mind while determining whether each word in the sentence was a noun. A response condition requiring alternation, in which participants were to tap

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with the left hand for nouns and the right hand for non-nouns (called the ‘‘tapping’’ condition), did not have a significant impact on the executively demanding verbal task. A recent study by Mitchell et al. (2002) provided evidence that spatial secondary tasks that are not executively demanding can disrupt letter n-back performance. In one experiment, a concurrent anti-saccade task, in which participants had to move their eyes horizontally away from a peripheral visual stimulus, was more disruptive of a letter n-back task than a concurrent no-saccade task, in which participants had to make no eye movements in response to the peripheral stimulus. The anti-saccade task is not a purely spatial task, as executive control is required to inhibit a reflexive response to foveate the peripheral stimulus. However, the nosaccade task was designed to match the executive requirements of the anti-saccade task, as the no-saccade task also required the inhibition of a reflexive response to foveate the peripheral stimulus. Thus, one can infer that the difference in n-back disruption was caused by the nonexecutive (e.g., spatial) processing requirements unique to the anti-saccade task. Further evidence for this interpretation was provided in a second experiment, in which a concurrent pro-saccade task and a concurrent anti-saccade task were equally disruptive of letter n-back performance. The only differences between the two saccade tasks were the executive requirements of the anti-saccade task, thus the executive requirements did not disrupt n-back performance. Remaining concerns about the certainty with which one can use a dual-task methodology to conclude that the letter n-back task recruits spatial processing were alleviated by the results of Experiment 3 of the current study, which indicated that spatial processing was occurring when the letter n-back task was done without a secondary task. Of course we have implicitly assumed that the eyes would not be as active during other verbal working memory tasks. Although further research is necessary to confirm this assumption, the results of Lawrence et al. (2001), who demonstrated that concurrent eye movements are disruptive of spatial working memory but not verbal working memory, are highly suggestive (for related evidence, see Baddeley, 1986). There are several other pieces of evidence that corroborate our hypothesis that the letter n-back task recruits spatial processing. First, PMd and right PPC, which are active during letter n-back tasks, are active in a variety of spatial tasks, including spatial working memory tasks (e.g., Courtney et al., 1996, 1998; Jonides et al., 1993; Prabhakaran et al., 2000; Reuter-Lorenz et al., 2000; Rowe et al., 2000; Smith et al., 1995, 1996; Zarahn et al., 1999, 2000), spatial motor tasks (e.g., Anderson et al., 1994; Connolly et al., 2000; Corbetta et al., 1998; Courtney et al., 1998; Fox et al., 1985; Luna et al., 1998; Nobre et al., 2000; Paus et al., 1993; Petit and Haxby, 1999; Petit et al., 1997; Sweeney et al., 1996), spatial attention tasks (e.g., Gitelman et al., 1999; Hopfinger et al., 2000; Kastner et al., 1999; Kim et al., 1999; LaBar et al., 1999; Nobre et al., 1997, 2000), and spatial cognition tasks (e.g., Lamm et al., 2001; Richter et al., 2000; Windischberger et al., in press). Second, verbal working memory tasks other than the letter n-back task do not activate PMd and right PPC (reviewed in D’Esposito et al., 1998). Third, a recent case study of a patient with right PPC damage (and a spatial processing deficit) reported deficits on a letter n-back task (Ravizza et al., 2003). An alternative to our view suggests that the PMd and right PPC activity in the letter n-back task supports the executive system rather than the spatial subordinate system (D’Esposito et al., 1998; Zurowski et al., 2002). However, the role of PMd and right PPC in

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spatial working memory is more consistent with the role of the spatial subordinate system (i.e., short-term storage) than the executive system (Smith and Jonides, 1999). For example, spatial working memory tasks that are not executively demanding activate PMd and right PPC (e.g., Courtney et al., 1996, 1998; Jonides et al., 1993; Prabhakaran et al., 2000; Reuter-Lorenz et al., 2000; Rowe et al., 2000; Smith et al., 1995, 1996; Zarahn et al., 1999, 2000). Also, increased executive demands in spatial working memory tasks do not produce increased activation in PMd and right PPC as they do in other areas more clearly associated with the executive system (Postle et al., 2000a). An important question concerns the specific role of spatial processing in the letter n-back task. Although the primary goal of our experiments was to answer a more general question concerning whether spatial processes in general were involved in the letter nback task, our results are informative concerning the specific role of spatial processes. In Experiment 1, repeated spatial responding was only required from the time the n-back decision was made until 500 ms before the onset of the next letter. In other words, spatial interference affected the maintenance (and perhaps, as discussed earlier, the updating) of the contents of working memory. Functions not affected by spatial interference include encoding the current letter, retrieving the n-back letter, comparing the current letter to the n-back letter, making a match decision, and making a differentiated response according to the decision; note, however, that the current results do not allow us to conclude that spatial processing is not involved in these functions. We can only speculate as to the specific role of spatial processing in maintenance and updating. Perhaps the letter sequences are mentally transformed into a spatial representation, and then rehearsed via the rehearsal mechanism of the spatial subordinate system (Awh and Jonides, 2001; Logie, 1995). The suggestion that nonspatial information can be represented spatially is not new to cognitive science (e.g., Bloom et al., 1996; Boroditsky, 2000; Hatano and Osawa, 1983; Lakoff and Nu´n˜ez, 2000; O’Keefe and Nadel, 1978; Shepard, 1982; Weinberg et al., 1972; Yates, 1966), and literate individuals would certainly be experienced with representing letters spatially. Concerning rehearsal, the results of Experiments 1 and 3 are consistent with the suggestion that spatial motor systems (e.g., those that control eye and arm movements) support the rehearsal component of the spatial subordinate system, just as the speech motor system supports the rehearsal component of the verbal subordinate system (Baddeley, 1986; Lawrence et al., 2001). The fact that PMd plays an important role in spatial motor control (e.g., Connolly et al., 2000; Graziano et al., 2002; Paus, 1996; Postle et al., 2000a; Schubotz and von Cramon, 2001) is also consistent with this suggestion. Another possibility (which is not mutually exclusive) is that spatial attention, which also activates PMd, supports the rehearsal component of the spatial subordinate system (Awh and Jonides, 2001). Verbal processing in the location n-back task In Experiment 4, we examined a possible role for the verbal subordinate system in the location n-back task (Fiez, 2001), and the results were consistent with this possibility. How might the verbal subordinate system aid location n-back performance? One possibility is that participants place verbal labels on to-be-remembered locations (Nystrom et al., 2000). For example, because the circular configuration of locations used in Experiment 4 resembles realworld objects such as a compass or a clock face, our participants

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could have used labels like ‘‘northeast’’ or ‘‘2 o’clock’’ as mnemonic aids. A recent study demonstrated that such verbal strategies were used in a color n-back task (Vuontela et al., 1999). The neuroimaging literature also provides evidence consistent with the possibility that the location n-back task recruits the verbal subordinate system. For example, the location n-back task, relative to other spatial working memory tasks, produces more left hemisphere activity (e.g., Carlson et al., 1998; Smith et al., 1996). Reconsidering conclusions drawn from research using the n-back task Our results raise questions about conclusions drawn in neuroimaging studies that have used the n-back task, especially concerning the domain generality and domain specificity of working memory. This is a very important issue, as the once dominant view, which emphasized domain-specificity of working memory in the frontal cortex of nonhuman primates (Goldman-Rakic, 2000; Wilson et al., 1993), has been vigorously challenged by human neuroimaging research, which has emphasized domain generality of working memory (D’Esposito et al., 1998; Miller, 2000). PMd and right PPC are two regions that may have been mischaracterized as domain-general by neuroimaging research. The bulk of the evidence suggests that these regions have spatial functions. We speculate that the PMd and right PPC activations found in n-back tasks using nonspatial stimuli are due to the spatial nature of the nback task, which was demonstrated in the current study. The verbal domain specificity of left frontal regions should also be reconsidered because claims that there are no verbal-specific regions in frontal cortex have been based primarily, if not exclusively, on the results of studies employing n-back tasks (D’Esposito et al., 1998; Nystrom et al., 2000; Zurowski et al., 2002).

would not normally be used to deal with information from another domain. For example, the verbal working memory task used by Brooks (1968), in which participants had to keep a sentence in mind while determining whether each word in the sentence was a noun or a non-noun, was more susceptible to interference from a spatial response (‘‘pointing’’) condition than from a nonspatial (‘‘tapping’’) response condition (although neither manual condition was as interfering as a verbal, or ‘‘vocal,’’ condition). We suspect that this is related to the fact that literate individuals are in the habit of representing sentences spatially. Engagement of the spatial subordinate system has also been implicated for a version of the digit span task in which the digits are to be recalled in reverse order (e.g., Hoshi et al., 2000; Rapport et al., 1994; Weinberg et al., 1972). The importance of task analysis Although functional neuroimaging has been an important development in cognitive neuroscience, it is not without limitations. Fortunately, these limitations can be overcome to some degree by using other tools in conjunction with neuroimaging. For example, PET or fMRI, which have poor temporal resolution, can be aided by combination with electroencephalography or magnetoencephelography, which have precise temporal resolution (Dale and Halgren, 2001). Similarly, concerns about whether neuroimaging results can be used to draw conclusions about a causal role of a particular brain region in a particular function can be addressed with converging evidence from neuropsychology or transcranial magnetic stimulation. Our results highlight the importance of using behavioral task analysis in conjunction with functional neuroimaging.

Recommendations for working memory task usage in neuroimaging

Acknowledgments

Decades of cognitive psychological and neuropsychological research have demonstrated the existence of subordinate systems that are specialized for maintaining specific domains of information (e.g., spatial, verbal, visual form). Thus, neuroimaging researchers have assumed, not unreasonably, that a working memory task involving, for example, verbal stimuli should only recruit the verbal subordinate system and the central executive. Our results suggest that the n-back task violates this assumption. For this reason, we recommend that neuroimaging researchers refrain from using the n-back task, at least when attempting to discriminate between domain-specific and domain-general processes, until further task analysis reveals exactly what processing components are engaged by different versions of the task. Since it was introduced to the neuroimaging literature (Cohen et al., 1994), the n-back task has been used almost exclusively by neuroimaging researchers interested in the executive system of working memory. Because we recommended that researchers temporarily refrain from using the n-back task when attempting to discriminate between domain-specfic and domain-general processes, we feel some obligation to recommend an alternative. Unfortunately, we are not aware of any executively demanding working memory tasks that have undergone a thorough task analysis. Moreover, we fear that other executively demanding tasks may be similar to the n-back task in their tendency to engage multiple subordinate systems. Executively demanding tasks may encourage the recruitment of subordinate systems that

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