Individual differences in executive attention and inhibitory control are related to spatial memory biases in adults

Abstract

Executive attention is involved in working memory; however, the role of executive attention in the maintenance of information in spatial working memory is debated. This study examined whether inhibitory control was related to spatial working memory biases in adults in a simple spatial memory task where participants had to remember one location on an otherwise blank computer screen. On some trials, a distractor was presented during the maintenance period. Eighty-four participants completed the spatial working memory task and a battery of cognitive control measures. When a distractor was presented during the maintenance period of the spatial memory task, performance on two of the cognitive control measures, a measure of overall attention and a measure of inhibitory control was related to memory errors. When a distractor was not presented during the spatial memory task, memory errors were not related to performance on the cognitive control tasks. Overall, these effects demonstrated that attention is related to maintaining locations in spatial working memory in adults, and inhibitory control may also be related such that those with more efficient inhibitory control were less influenced by distractors presented during the maintenance period.

Keywords

Spatial working memory attention inhibitory control

Introduction

Working memory involves maintaining information in memory to complete a task (Miyake & Shah, 1999) and is essential for interacting with the world. Although we have some knowledge of the cognitive processes and brain areas that are involved in working memory, we still do not have a complete understanding of the processes involved. For example, executive attention, defined as the top-down control of attention, is involved in encoding information into working memory (Engle, 2002), but less is known about how it is involved in the simple maintenance of information in working memory (Kane et al., 2007; Lewis-Peacock et al., 2012; Oberauer, 2019). Research is mixed, but suggests that after encoding and consolidation, executive attention may not be required for maintaining information in verbal or visual working memory when the memory task is simple (see Oberauer, 2019 for a review), although a task that requires more complex processing during maintenance requires executive attention (McCabe et al., 2010). Spatial working memory (SWM), however, appears to be different, with executive attention involved even during maintenance in simple spatial memory tasks (e.g., Lawrence et al., 2004).

Several lines of research have found that executive attention may be involved in maintenance of locations in spatial working memory. Studies of spatial working memory that use a spatial span task, such as the Corsi blocks task, find that shifts of attention during the maintenance period interfere with memory performance (Klauer & Stegmaier, 1997; Lawrence et al., 2004; Smyth & Scholey, 1994), as does a simultaneous secondary task that involves executive attention (Klauer & Stegmaier, 1997; Rudkin et al., 2007). Wu (2020) also found that measures of visual attention correlated with spatial working memory span in young children. In addition, when maintaining just one location in memory, such as remembering a location on a computer screen, memory performance was influenced by completing a secondary task during the maintenance period that required an attentional shift (Awh & Jonides, 2001; Johnson & Spencer, 2016). Notably, these shifts of attention biased memory responses towards the attended location, rather than just lowering accuracy (Johnson & Spencer, 2016). This bias suggested that the location of the attentional shift interacted with the target location being held in memory.

Distractors presented during the maintenance period also influence memory. Distractors can bias memory either towards or away from the distractor location or increase error without causing a significant bias, depending on the details of the task. Schutte and DeGirolamo (2020) had participants remember one target location on each trial and presented a distractor during the maintenance period. The memory responses of the participants were biased away from the distractor location when the distractor location was near the target location and were not biased when the distractor was far from the target location. Using a multiple object tracking task, Liverence and Scholl (2011) also found that targets were remembered as being biased away from distractors. They called this bias an inhibitory expansion effect. In contrast, however, other studies using tasks similar to the task used by Schutte and DeGirolamo found that memory responses were biased towards the distractor location (Herwig et al., 2010; Van der Stigchel et al., 2007) or not significantly biased by the distractor (Marini et al., 2017).

The reason for this difference in the direction of the bias has not been determined, but the difference may be due to whether the distractor captures attention, because memory responses are biased towards attended locations in tasks that require attentional shifts (Awh & Jonides, 2001; Johnson & Spencer, 2016), or whether participants are able to suppress the distractor location either pre-attentively or very soon after attention is captured. This suppression may cause memory responses to be biased away from the distractor location when the distractor is near the target location.

Studies of visual attention suggest that participants can suppress sudden onsets in certain contexts. The signal suppression hypothesis proposes that top-down, executive control mechanisms can suppress salient stimuli that do not match the features of the target stimuli (see Gaspelin & Luck, 2018). Using electroencephalography (EEG) and a visual working memory task, Hakim et al. (2021) tested whether distractors presented during the memory delay were encoded into working memory. They found that distractors were encoded into working memory only when they were task-relevant (i.e., they had to complete a secondary task discriminating the colour of the distractor); distractors that could be ignored initially captured spatial attention, but then were suppressed and did not enter working memory. In visual search tasks, if the distractor was always the same or if the participant was told what the distractor would be (e.g., what colour), participants could also actively ignore distractors and reaction times were faster (see Geng et al., 2019 for a review).

In a spatial working memory task, suppression of a distractor by top-down inhibitory mechanisms may result in a bias away from the distractor location. If participants are relying on inhibitory control to actively suppress, or inhibit, the distractor, individual differences in memory biases should be related to individual differences in inhibitory control. Beattie et al. (2018) examined this in children and found that the memory responses of children with higher levels of inhibitory control were biased more strongly away from distractors that were presented during the maintenance period of the memory task. This relationship, however, may be stronger in children than adults, because working memory and inhibitory control are less differentiated in children (Wiebe, et al., 2008; Wiebe et al., 2011). The current study tested whether measures of inhibitory control were related to biases away from distractors in adults. If so, this relationship would suggest that top-down, cognitive control mechanisms are involved in maintaining a location in spatial memory.

When remembering a target location in a homogeneous space, there is a second type of memory bias that is related to the boundaries and symmetry axes of the space (Huttenlocher et al., 1991). For example, adults use the vertical symmetry axis when remembering a location in a rectangular space, such as a rectangular computer monitor (Spencer & Hund, 2002, 2003), and their memory responses are biased away from the vertical symmetry axis of the monitor (Simmering et al., 2006). These types of biases have been called geometric biases, and they increase as the memory delay increases (Schutte & Spencer, 2009). The dynamic field theory (DFT) of spatial memory uses dynamic neural fields to model working memory and explains these biases as the result of the interaction of the perceived midline symmetry axis and the maintained location in working memory (Schutte & Spencer, 2009; Simmering et al., 2008). In the model, the target location is maintained in a working memory neural field through a local activation and lateral inhibition function. The strength of the lateral inhibition increases over development, which results in smaller geometric biases and lower variability, i.e., a more stable memory (Schutte & Spencer, 2009; Wu & Schutte, 2020). Beattie et al. (2018) tested whether inhibitory control was related to geometric biases in children. They found that children with higher levels of inhibitory control were less biased away from the midline symmetry axis, i.e., smaller geometric biases. This relationship suggests that, at least for children, inhibitory control is involved in maintaining the target location during the memory delay, even when distraction is minimal. This relationship has not been tested in adults, however. If inhibition is involved in the simple maintenance of a location in memory, greater inhibition should be related to smaller geometric biases in adults, although the type of inhibitory control that is measured may affect this relationship.

While inhibitory control may be homogeneous in children, it appears to be differentiated into multiple types in adults, and these different types involve different neural circuitry (Aron et al., 2007; Goldstein et al., 2007). Just defining inhibitory control and separating it from executive attention is a challenge (MacLeod et al., 2003). For example, in many selective attention tasks, such as visual search tasks, suppressing distractors does not appear to rely on top-down inhibitory mechanisms (see van Moorselaar & Slagter, 2020 for a review). In addition, behavioural measures of inhibitory control often do not correlate strongly with each other, and factors extracted from factor analyses are often driven by one task (Rey-Mermet et al., 2018). In addition, inhibition can be differentiated in several different ways, such as into response inhibition, resistance to distracters, and resistance to proactive interference (Friedman & Miyake, 2004), but the differences are not always clear. For example, response inhibition and resistance to distracters appear to be strongly related, such that they are either considered to be the same factor (Friedman & Miyake, 2004; Pettigrew & Martin, 2014) or separate, but strongly related, factors (Rey-Mermet et al., 2018; but see also Stahl et al., 2014).

Due to differences in relationships between different measures of inhibitory control, we used a battery of inhibitory control measures, including behavioural measures and a self-report measure, to test the relationship between spatial working memory biases and inhibitory control in adults. Specifically, we used a visual Simon task, a cued go–no-go task, a Stroop task, and the Barrett Impulsivity Scale (BIS). We chose a go–no-go task, because Beattie et al. (2018) found a relationship between performance on a go–no-go task and spatial memory in children; however, research in adults suggests that the simple go–no-go task relies on automatic inhibition (Verbruggen & Logan, 2008) rather than top-down inhibitory control. Therefore, we chose a cued go–no-go task and analysed the trials with a go cue and no-go response as a measure of top-down inhibitory control. We chose the visual Simon task, because it involves a spatial component: participants respond to the stimulus based on colour while inhibiting responding based on its location on the screen. We chose the colour Stroop, because it is a commonly used measure of inhibitory control.

The first goal of this study was to replicate the bias away from distractors that were close to the target location (Schutte & DeGirolamo, 2020). Based on Schutte and DeGirolamo, we predicted that memory responses would be biased away from the distractors with the strongest biases for the distractors that were closest to the target location. The second goal was to test the following hypotheses: (a) better inhibitory control would be related to smaller biases away from midline, i.e., a more stable memory and (b) better inhibitory control would be related to larger biases away from distractors, i.e., greater suppression of the distractor.

Method

Participants

Eighty-four undergraduate students (M_age = 20.29 years, SD = 5.17 years, 27 males, 54 females, and three did not disclose gender) participated in this study for course credit. Data from one participant were not recorded due to computer errors, so that participant was excluded from analyses. All participants reported normal or corrected-to-normal vision and gave written informed consent prior to data collection. This study was approved by the University of Nebraska–Lincoln Institutional Review Board and was conducted in accordance with the ethical standards as stated in the 1964 Declaration of Helsinki and its later amendments.

Materials

All tasks were completed on a black 39.5″ Sharp LED monitor with a resolution of 1920 × 1200. The monitor was tilted up 15 degrees from horizontal. The keyboard, while in use, was temporarily mounted on a wooden rail located directly in front of the monitor at the same height as the monitor. Stimuli for the spatial memory task were presented using E-Prime 2.0 while all other tasks and questionnaires used Inquisit.

Procedure

After providing informed consent participants sat down in a chair that was kept a fixed 25 inch distance from the monitor. Once seated, the participants started one of four possible computer tasks. The order of the tasks was randomised to avoid order effects. Participants remained seated throughout the entire experiment. Following the completion of the computer tasks, the participant answered the BIS and a background questionnaire.

Tasks

Spaceship Spatial Memory Task

Participants completed the spatial memory task in a dim room with black curtains around the walls to prevent them from using any landmarks in the room as memory aids (Schutte & Spencer, 2009). Stimuli were presented on an otherwise black computer screen. Each participant began the task with a demonstration trial where the researcher walked them through task expectations step by step. Participants then completed two practice trials to confirm that they understood the task. After the practice trials, they completed the experimental trials. Each trial started with an audio prompt saying, “Let’s look for a spaceship.” The target, a 1 cm blue triangle representing the spaceship, appeared for 2,000 ms at one of two possible locations on the computer monitor. Participants were instructed to continue sitting straight up with no hovering over the location of the target until the computer said “go, go, go.” Correct posture was ensured during the task via constant monitoring of the participant by the researcher. At the “go” prompt, participants used a stylus to double tap the location at which they remembered seeing the target. On most of the trials the “go” prompt occurred 10 s after the target disappeared. On four trials, the go signal occurred as soon as the target disappeared. These no delay trials were used to confirm that the touchscreen was calibrated correctly and were not included in the analyses. Two-thirds of the trials included a 1 cm yellow, circular “distractor” that appeared 7,500 ms after the target disappeared and remained on the screen for 1,000 ms. The “go” prompt was 1,500 ms after the distractor disappeared (see Figure 1). Participants were instructed to ignore the distractors. Following the participant response, the computer gave auditory feedback indicating whether their response was on the target location, was close to the target location, or was far from the target location.

Targets could appear at one of two locations, depending on condition. Each participant was randomly assigned to one of two conditions for this task. Individuals in one condition saw targets appear −20° and 40° from midline and individuals in another condition saw targets −40° and 20° from midline (see Figure 2). Distractors were presented either 5° or 12.5° inside or outside the target location relative to the vertical symmetry axis of the monitor. Thus, distractor locations were −7.5°, –15°, –25°, –32.5° for the −20° target, 27.5°, 35°, 45°, and 52.5° for the 40° target, –27.5°, –35°, –45°, and −52.5° for the −40° target and 7.5°, 15°, 25°, and 32.5° for the 20° target. Participants completed five trials for each distractor (four distractor locations and no distractor trials) and target (two target locations) combination for a total of 50 experimental trials.

Colour Stroop task

Colour words were presented in the centre of the screen and participants were asked to indicate the colour of the font by pressing a key while inhibiting the meaning of the word (Jensen & Rohwer, 1966). Participants were instructed to respond as quickly, yet as accurately, as possible. There were four possible key responses: D, F, J, and K to indicate red, green, blue, and black, respectively. In the task, there were multiple congruency types. A congruent trial was when the colour of the font and meaning of the word were the same, an incongruent trial was when the colour of the font and meaning of the word were not the same, and a control trial was when a rectangle was presented instead of a word and participants responded to the colour of the rectangle. Each combination of trial type (congruent, incongruent, and control) and colour was used seven times for a total of 84 trials. The trial order was randomised. All stimuli remained on the screen until a response was made, there would then be either an intertrial interval of 200 ms or, if an error was made, feedback was given for 400 ms before the next trial.

Cued go/no-go task

Participants completed a cued go/no-go task (Fillmore, 2003) where they were instructed to respond to or not respond to the target based on the colour of the target. In this task, a “go” target was a green rectangle and a “no-go” target was a blue rectangle. When a go target was presented on the screen, participants responded by pressing the spacebar on the mounted keyboard in front of them as quickly as possible. These targets were preceded by a cue in the form of a blank rectangle. This rectangle was outlined in black but filled in with white to match the background screen colour. All rectangles presented were vertical or horizontal. The orientation of the cue rectangle indicated what type of cue it was. Eighty per cent of the vertical cues were followed by a go trial. Eighty per cent of the horizontal cues were followed by a no-go trial. Therefore, a vertical rectangle was considered a go cue and a horizontal rectangle was considered a no-go cue. At the start of a trial participants were presented with a fixation cross in the centre of the screen for a duration of 800 ms followed by a blank screen for 500 ms before the presentation of the cue. Each cue would be presented for a varying amount of time prior to the onset of the target. There were five stimulus onset asynchrony (SOA) options which dictated the time between when the cue was presented and when the target would appear on the screen: 100, 200, 300, 400, and 500 ms that were randomised. Each participant completed a total of 250 trials with 20 go cue/go target trials, five go cue/no-go target trials, 20 no-go cue/no-go target trials, and five no-go cue/go target trials for each SOA.

Visual Simon task

Participants began the task (Simon & Wolf, 1963) by completing at least eight practice trials. If a mistake was made on any of these eight trials, participants completed additional practice trials until a total of eight trials were completed without error. Individuals then completed 28 test trials. At the start of a trial, a fixation cross appeared in the centre of the screen for 800 ms. The cross was followed by a 250 ms blank interval. The target then appeared on either the right or left side of the screen and remained there until a response had been made or until 1,000 ms passed with no response. This target would be either a blue or red square. If the target was blue, participants were instructed to respond by hitting the left “shift” key, and they were instructed to hit the right “shift” key if the target was red. Half of the experimental trials were congruent, i.e., the square was presented on the same side as the correct response key, and half of the experimental trials were incongruent, i.e., the square was presented on the opposite side of the correct response key. The order of trials was randomised.

Barratt Impulsiveness Scale (BIS-11)

The BIS (Patton et al., 1995) consisted of 30 items that described impulsive and non-impulsive behaviours. Participants were instructed to score these items on a 4-point scale where 1 represented rarely/never and four represented almost always/always. Examples of statements detailing impulsive behaviour included “I act of the spur of the moment” and “I spend or charge more than I earn” while non-impulsive behaviour statements were “I plan tasks carefully” and “I save regularly.” Participants could score between 30 and 120. Higher scores indicated greater impulsivity.

Demographic questionnaire

Participants completed a questionnaire containing ten demographic-type questions. Examples of topics included age, gender, and the type of environment the participant grew up in.

Data analytic strategies

To address reliability issues with using response time difference scores in inhibitory control tasks (Draheim et al., 2019), we computed the reliabilities for the different potential variables that involved an inhibitory component and used the measure that provided the greatest level of reliability (see Table 1 for reliabilities of different inhibitory control measures). For percent correct, we computed split-half reliabilities and for response time differences, we used the formula in Draheim et al. (2019). For the visual Simon task, we chose accuracy on the congruent trials and incongruent trials. Performance on the congruent trials is included to act as a control for general executive attention, and performance on the incongruent trial is a measure of inhibitory control. For the go–no-go task, we chose accuracy on the go cue–no-go trials. Accuracy on the trial types where the cue was congruent with the response was near or at ceiling, so we did not compute a difference score. For the Stroop task, reliabilities for all of the variables were below .70, so that, we chose the reaction time difference score between the incongruent trials and the control trials, which had the highest reliability (see Table 2 for variable names). We removed outliers that were three standard deviations above a participant’s mean response time in the colour Stroop task (95 trials, 1.3%) and response times that were less than 200 ms (six trials, 0.08%). We conducted a factor analysis to examine whether a composite score should be used. Results showed that the variables were moderately to highly independent and factors generated were not able to capture the majority variance among the variables. This suggested that a composite score should not be used; therefore, we used each inhibitory control variable in the analyses.

Table 1.

Reliability of measures in the inhibitory control tasks.

Measures	Reliability
Simon congruent	0.74
Simon incongruent	0.73
Simon RT difference	0.15
Stroop congruent	0.43
Stroop incongruent	0.38
Stroop control	0.41
Stroop RT difference	0.59
G/NG go cue–no-go trials	0.86
G/NG RT difference	0.67

G/NG: go/no go; RT: Response time.

Table 2.

Measurements from the inhibitory control tasks.

Variable names
Simon incongruent	Percent correct in the incongruent trials in the visual Simon task
Simon congruent	Percent correct in the congruent trials in the visual Simon task
G/NG	Percent correct in the go cue—no-go trials in the go/no–go task
Stroop	Response time differences between incongruent and control trials in the Colour Stroop task
BIS	Scores from the Barrett impulsivity scale
Gender	Gender

G/NG: Go/no-go; BIS: Barrett impulsivity scale.

For the spaceship spatial memory task, the computer recorded two taps of the stylus on the screen. Thus, if a participant’s first touch was not where they intended, they could respond a second time. The computer calculated the absolute distance in millimetres between each touch and the target location, and the touch closest to the target was used in the analyses. Outliers more than 3 standard deviations from the mean absolute error were removed (37 trials, 0.9%). Constant directional errors in degrees were computed for the remaining trials. Directional errors towards midline were coded as negative and errors away from midline were coded as positive (see Figure 2).

We used hierarchical linear modeling (HLM) 8.0, R 4.1.1, and SAS statistical software to analyse the data. The multilevel models used listwise deletion, so that, six participants who did not have complete data were not included in the multilevel models. Three were excluded because they did not report gender, one did not complete the go/no-go task and one who did not complete the BIS due to a computer issue. Inspection of the data also revealed one participant from the go/no-go task who made a larger than expected number of errors (above 50% errors), so that, the data were excluded.

Results

Means and standard deviations of study variables are shown in Table 3. Correlations are shown in Table 4. Mean constant error on the no distractor trials was positive, or, in other words, biased away from the midline symmetry axis of the monitor. To test the hypothesis that the bias away from distractors varied by the specific distractor location compared to no distractor, we analysed constant directional error for each trial using Proc Mixed in SAS. We used a compound symmetry covariance structure for the model. The model included main effects for target (20°, 40°) and distractor condition (−12.5°, −5°; no distractor, 5°, 12.5°) and their interaction. Trial number, gender, and condition were entered as control variables. Restricted maximum likelihood (REML) was used in reporting model parameters, and degrees of freedom were calculated using the containment method. The only significant effect was a main effect of distractor condition, F (3,332) = 18.77, p < .0001.

Table 3.

Means and standard deviations of study variables.

Variables	n	M	SD
BIS	83	56.89	10.03
Simon congruent	84	0.95	0.06
Simon incongruent	84	0.95	0.08
Stroop	83	192.61	161.26
Go/no go	82	0.99	0.02
SWM (no distractor)	84	2.07	1.72
SWM (distractor)	84	0.49	0.78

BIS: Barrett impulsivity scale; SWM (no distractor): spatial working memory trials without distractor; SWM (distractor): spatial working memory trials with distractor.

Table 4.

Correlations between study variables.

	1	2	3	4	5	6
1. BIS
2. Simon congruent	0.06
3. Simon incongruent	−0.14	0.30**
4. Stroop	−0.27*	0.17	0.12
5. G/NG	−0.17*	0.12	0.01	0.04
6. SWM (no distractor)	0.03	−0.06	0.03	0.04	−0.06
7. SWM (distractor)	−0.03	0.22	0.27*	0.20	−0.05	0.12

BIS: Barrett impulsivity scale; G/NG: go/no go; SWM (no distractor): spatial working memory trials without distractor; SWM (distractor): spatial working memory trials with distractor.

p < .05, **p < .01.

The influence of distractor on constant directional error can be seen in Figure 3. For the figure, we computed the difference between mean constant directional error on the no distractor trials and the distractor trials for each of the distractor locations. Biases away from the distractor are positive difference scores, and biases towards the distractor are negative. As can be seen in the figure, mean difference scores were all positive, indicating biases away from the distractor locations. We examined the differences of least square means within Proc Mixed to determine which distractor locations were significantly different from no distractor trials. When the distractor was at −12.5° or −5° relative to the target location, constant directional error did not differ from the no distractor trials, −12.5°: t (332) = 1.27, p = .206; −5°: t (332) = 1.63, p = .103, however, memory responses were significantly biased away from both the 5° and 12.5° distractor locations, 5°: t (332) = 5.66, p < .0001; 12.5°: t (332) = 2.65, p = .009.

The relationship between inhibitory control and spatial memory biases on no distractor trials

We used multilevel models to test the relationship between inhibitory control and spatial memory biases away from the vertical symmetry axis on no distractor trials. Target location was implemented at Level 1 and was dummy coded (0 = ± 20°, 1 = ± 40°) and uncentred. Level 2 variables are listed in Table 2 and were grand mean centred, except for gender (uncentred; dummy-coded; 0 = male, 1 = female). The multilevel models were the following.

Level 1 model:

S p a t i a l m e m o r y b i a s e s_{i j} = β_{0 j} + β_{1 j} * (t a r g e t_{i j}) + r_{i j}

Level 2 model:

\begin{matrix} β_{0 j} = γ_{00} + γ_{01} * (S i m o n I n c o n g r u e n t_{j}) + \\ γ_{02} * (S i m o n C o n g r u e n t_{j}) + γ_{03} * (G / N G_{j}) + \\ γ_{04} * (S t r o o p_{j}) + γ_{05} * (B I S_{j}) + γ_{06} * (g e n d e r_{j}) + u_{0 j} \\ β_{1 j} = γ_{10} + γ_{11} * (S i m o n I n c o n g r u e n t_{j}) + \\ γ_{12} * (S i m o n C o n g r u e n t_{j}) + γ_{13} * (G / N G_{j}) + \\ γ_{14} * (S t r o o p_{j}) + γ_{15} * (B I S_{j}) + γ_{16} * (g e n d e r_{j}) + u_{1 j} \end{matrix}

Results are shown in Table 5. Gender was a significant predictor of spatial memory biases, unstandardised coefficient = –1.64, SE = 0.62, t = –2.64, p = .01. This result indicated that females displayed smaller spatial memory biases away from the vertical axis than males. None of the measures of inhibitory control were significant predictors of spatial memory biases on no distractor trials.

Table 5.

Results of multilevel models for spatial memory biases on no distractor trials.

Fixed effect	Coefficient	SE	t-ratio	df	p-value
Intercept, β₀
γ₀₀	3.23	0.51	6.30***	71	< .001
γ₀₁ (Simon Incongruent)	1.52	4.62	0.33	71	.744
γ₀₂ (Simon Congruent)	−0.93	4.20	−0.22	71	.826
γ₀₃ (G/NG)	−5.66	12.61	−0.45	71	.655
γ₀₄ (Stroop)	0.00	0.00	1.01	71	.318
γ₀₅ (BIS)	−0.02	0.03	−0.82	71	.416
γ₀₆ (gender)	−1.64	0.62	−2.64*	71	.010
Target slope, β₁
γ₁₀	−1.26	0.67	−1.88	71	.064
γ₁₁ (Simon incongruent)	2.70	7.11	0.38	71	.705
γ₁₂ (Simon congruent)	0.16	6.32	0.03	71	.980
γ₁₃ (G/NG)	5.75	14.92	0.39	71	.701
γ₁₄ (Stroop)	−0.00	0.00	-1.02	71	.310
γ₁₅ (BIS)	0.05	0.03	1.55	71	.125
γ₁₆ (gender)	1.62	0.83	1.96	71	.055

SE: standard error; G/NG: go/no go; BIS: Barrett impulsivity scale.

p < .05. ***p < .001.

The relationship between inhibitory control and spatial memory biases on distractor trials

We then tested whether inhibitory control was related to spatial memory biases on distractor trials. The multilevel models were the same as the previous models except that the dependent variable was the differences in spatial memory error between distractor and no distractor trials, and the distractor variable was added to Level 1 of the multilevel (MLM) model. Distractor locations included −12.5°, –5°, 5°, and 12.5°, and was group mean-centred.

Level 1 Model:

\begin{array}{l} D i f f e r e n c e s i n \\ s p a t i a l m e m o r y b i a s e s_{i j} = β_{0 j} + β_{1 j} * (t a r g e t_{i j}) + \\ β_{2 j} * (d i s t r a c t o r_{i j}) + r_{i j} \end{array}

Level 2 Model:

\begin{matrix} β_{0 j} = γ_{00} + γ_{01} * (S i m o n I n c o n g r u e n t_{j}) + \\ γ_{02} * (S i m o n C o n g r u e n t_{j}) + γ_{03} * (G / N G_{j}) + \\ γ_{04} * (S t r o o p_{j}) + γ_{05} * (B I S_{j}) + \\ γ_{06} * (g e n d e r_{j}) + u_{0 j} \\ β_{1 j} = γ_{10} + γ_{11} * (S i m o n I n c o n g r u e n t_{j}) + \\ γ_{12} * (S i m o n C o n g r u e n t_{j}) + γ_{13} * (G / N G_{j}) + \\ γ_{14} * (S t r o o p_{j}) + γ_{15} * (B I S_{j}) + γ_{16} * (g e n d e r_{j}) \\ β_{2 j} = γ_{20} + γ_{21} * (S i m o n I n c o n g r u e n t_{j}) + \\ γ_{22} * (S i m o n C o n g r u e n t_{j}) + γ_{23} * (G / N G_{j}) + \\ γ_{24} * (S t r o o p_{j}) + γ_{25} * (B I S_{j}) + γ_{26} * (g e n d e r_{j}) \end{matrix}

The results are shown in Table 6. Performance on the visual Simon task congruent trials was related to spatial memory bias differences between distractor trials and no distractor trials, unstandardised coefficient = 3.55, SE = 1.63, t = 2.17, p = .033. Specifically, greater accuracy in the visual Simon congruent trials was associated with greater memory bias differences. Performance on the go/no-go task was significantly related to memory bias differences and this relationship varied by distractor location, unstandardised coefficient = –0.89, SE = 0.41, t = –2.15, p = .032. Further exploration of this interaction effect showed that when the distractors were at 5° and 12.5°, i.e., distractors were located outside of the target relative to midline, greater inhibitory control in the go/no-go task was associated with smaller memory biases differences. To graph this relationship in, we divided participants into two groups based on performance in go/no-go task (see Figure 4). The first group were correct on all the go cue-no-go trials, and the second group made errors on the go cue–no-go trials. We graphed the difference score for each group for each distractor. As can be seen in the figure, participants who were accurate in the go/no-go task displayed smaller spatial memory biases away from distractors than those were less accurate on the go/no-go task and this effect was larger for the 5° distractor than for the 12.5° distractor.

Table 6.

Results of multilevel models for spatial memory biases on distractor trials.

Fixed effect	Coefficient	SE	t-ratio	df	p value
Intercept, β₀
γ₀₀	0.48	0.22	2.18*	71	0.032
γ₀₁ (Simon incongruent)	0.60	1.22	0.49	71	0.624
γ₀₂ (Simon congruent)	3.55	1.63	2.17*	71	0.033
γ₀₃ (G/NG)	−4.95	4.03	−1.23	71	0.223
γ₀₄ (Stroop)	0.00	0.00	1.19	71	0.239
γ₀₅ (BIS)	−0.00	0.01	−0.33	71	0.742
γ₀₆ (gender)	0.13	0.23	0.56	71	0.579
Target slope, β₁
γ₁₀	0.00	0.24	0.00	531	0.997
γ₁₁ (Simon incongruent)	1.18	1.72	0.69	531	0.494
γ₁₂ (Simon congruent)	−3.34	2.31	−1.45	531	0.149
γ₁₃ (G/NG)	3.91	4.66	0.84	531	0.402
γ₁₄ (Stroop)	0.00	0.00	0.06	531	0.951
γ₁₅ (BIS)	0.01	0.01	0.52	531	0.606
γ₁₆ (gender)	−0.12	0.30	−0.41	531	0.683
Distract slope, β₂
γ₂₀	0.06	0.01	3.43***	531	< 0.001
γ₂₁ (Simon incongruent)	0.20	0.16	1.23	531	0.218
γ₂₂ (Simon congruent)	−0.28	0.29	−0.99	531	0.325
γ₂₃ (G/NG)	−0.89	0.41	−2.15*	531	0.032
γ₂₄ (Stroop)	0.00	0.00	0.08	531	0.938
γ₂₅ (BIS)	0.00	0.00	0.25	531	0.804
γ₂₆ (gender)	−0.03	0.02	−1.02	531	0.306

SE: standard error; G/NG: go/no go; BIS: Barrett impulsivity scale.

p < .05. **p < .01. ***p < .001.

Discussion

The first goal of this study was to replicate the memory bias away from distractors found by Schutte and DeGirolamo (2020). Memory responses were biased away from the distractors that were outside of the target relative to the midline symmetry axis of the monitor, and the strongest bias away was caused by the distractor that was closest to the target location. Memory responses on the trials with distractors that were between the target location and the midline of the monitor were also biased away from the distractors, but the bias was small and did not reach significance. This pattern of bias generally replicates the findings of Schutte and DeGirolamo, although the bias away from distractors that were between the target location and the midline of the monitor was significant in that study. The difference between the two studies may be due to a slightly smaller sample size in the current study (Schutte and DeGirolamo had over 120 participants), or it may be due to participants completing one less trial for each distractor-target combination in this study, five in this study versus six in Schutte and DeGirolamo. Although memory responses were not significantly biased away from all distractors, the pattern of bias replicated that of Schutte and DeGirolamo.

We also tested two hypotheses about the relationship between inhibitory control and spatial working memory biases. The first hypothesis was that higher levels of inhibitory control would be related to smaller spatial memory biases away from the midline axis, i.e., a more stable memory. Results did not support this hypothesis. This result differs from Beattie and colleagues (2018), who found that inhibitory control was related to geometric biases in children. These findings suggest that inhibitory control may not be involved in maintaining a single location in memory for adults, or that the measures of inhibitory control the adults completed in this study did not capture the type of inhibitory control used by adults when maintaining a location in memory. This finding needs to be replicated and explored further. Future research should include an oculomotor inhibition task to further explore how different types of inhibition are related to spatial memory.

An unpredicted finding was that gender was related to geometric biases in spatial memory in the model examining the relationship between inhibitory control and spatial memory biases away from the vertical symmetry axis on the no distractor trials. Gender was not significant in the analysis of the spatial working memory data alone, but that analysis involved both no distractor and distractor trials. Interestingly, the memory responses of females were less biased away from midline than those of males. Previous research that analysed gender found that females showed greater spatial memory biases than males (e.g., Holden et al., 2015) or there were no gender difference in biases (e.g., Schutte & DeGirolamo, 2020). Given the difference in findings from previous research, and that we did not have an equal number of males and females, this gender difference should be viewed sceptically unless it is replicated.

The second hypothesis was that greater inhibitory control would be related to a greater bias away from the distractor due to stronger inhibition, or suppression, of the distractor in the spatial working memory task. Rather than being related to the inhibitory control measures, higher accuracy on the congruent trials of the visual Simon task, our measure of general executive attention, was related to greater bias away from distractors. The incongruent trials, however, were not related to biases from the distractors. This finding suggests that general executive attention may be related to suppression of the distractor. There was also a significant relationship between spatial memory biases caused by the distractor and performance on the go cued no-go trials in the go–no-go task, but it was opposite of the predicted direction. Performance on the cued go–no-go trials was related to smaller biases away from the distractor. This finding supports the idea that inhibition is involved in maintaining a location in working memory in the face of distractors, but not in the way proposed by the hypothesis. It is possible that most adults can inhibit the distractor when instructed to do so, but those with better inhibitory control more efficiently suppress the distractor, and, as a result, their memory for the target is not as strongly influenced by the distractor.

This finding also differs from the findings of Beattie et al. (2018). Beattie and colleagues found that young children who had higher levels of inhibitory control, as measured by parental report, were biased away from distractors that were outside of the target location relative to the midline of the monitor. This difference in the relationship between inhibitory control and biases away from distractors may be due to the two studies using different measures of inhibitory control, but it is also possible that inhibiting a distractor is more difficult for children so some are able to inhibit it and some cannot inhibit it. In contrast, the majority of adults may be able to inhibit a distractor, but vary on how efficiently they are able to inhibit it.

Overall, the results of this study provide some support for theories of spatial working memory that propose that inhibitory control is involved in the maintenance of locations in spatial working memory, and not just the encoding of locations. However, not all measures of inhibition were related to spatial working memory. Moreover, not all measures of inhibition were related to each other. This could be due to issues with reliability. Difference scores, in particular, have been shown to not be very reliable (Draheim et al., 2019); however, even measures of accuracy, which were reliable in our study, were not strongly correlated. This lack of relationship could also be due to the tasks measuring different types of inhibition. Although all of the tasks purportedly measured response inhibition, they differ in that the go–no-go task was the only task where a cue was given prior to the target which would have resulted in suppressing an already prepared response when the no-go target was presented. In the other tasks, interference occurred at the same time as the preparation of the response. Perhaps this difference resulted in the cued go–no-go trials being a better measure of top-down inhibitory control than the other inhibitory control measures. Future research should examine different measures of top-down inhibitory control and executive attention to determine which are most strongly related to spatial working memory biases.

Future research should also explore what factors determine whether a distractor is suppressed or attended. Schutte and DeGirolamo (2020) varied the timing of the distractor and found that memory responses were biased away from distractors even when they were displayed for only 500 ms. Eye movements, however, were not controlled in the current study, or in Schutte and DeGirolamo, so participants could foveate the target and the distractor. Eye movements have been found to lower accuracy of spatial memory (Postle et al., 2006), but future research should examine whether eye movements also influence spatial memory in a more subtle way, i.e., by changing the influence of a distractor on spatial memory biases.

This study had several limitations. First, like in many studies that use a college-student sample, there were more females than males in the study. Given the gender difference found here future research should more carefully control the number of males and females. Second, not all measures of cognitive control were related to spatial memory biases, despite not all of them being significantly correlated with each other. Future research should replicate these findings and explore different measures of inhibitory control, such as oculomotor inhibitory control, to determine what type of inhibitory control is related to maintaining locations in spatial working memory.

Conclusion

This study replicates the spatial memory biases away from distractors found by Schutte and DeGiroloamo (2020) as well as others (e.g., Liverence & Scholl, 2011). The significant relationships between individual differences in executive attention, inhibitory control and spatial memory biases suggest that executive attention and inhibitory control are involved in maintenance of a location in memory, even in a simple spatial memory task. The relationship between inhibitory control and spatial memory biases has implications for theories of spatial working memory. Future research should delve deeper into the relationship between spatial memory biases and inhibitory control using eye-tracking and neuroimaging methods. Understanding the mechanisms underlying spatial memory is important for developing a better understanding of deficits in cases of head injuries (e.g., Lehnung et al., 2001) or developmental disorders, such as Attention Deficit Hyperactivity Disorder (ADHD) (e.g., Sowerby et al., 2011).

Footnotes

Acknowledgements

The authors would like to thank the research assistants who helped with collecting data for this study.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Anne R Schutte

Data availability statement

The datasets generated and analysed during the current study are not publicly available due to IRB limitations but are available from the corresponding author on reasonable request.

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