Do Inhibitory Control Demands Affect Event-Based Prospective Memory Performance in ADHD?

Abstract

Objective: Empirical evidence on prospective memory (PM) in ADHD is inconsistent. Differential findings have been related to differential executive control demands. This study aimed at exploring the impact of inhibitory control on event-based PM performance in ADHD. Method: Eighteen adults with ADHD and 18 controls performed a word categorization task with an embedded event-based PM task. In addition, participants performed an acoustically presented task that put either low or high loads on inhibitory control processes. Results: Inhibitory load did not differentially affect PM performance: Across both inhibitory load conditions, individuals with ADHD showed reduced PM performance when compared with controls. Moreover, inhibitory load did not influence PM performance across both groups. Conclusion: Possibly, full inhibitory control resources are not necessary during the entire duration of an event-based PM task, but may suffice to be employed after cue detection when needing to interrupt the ongoing task. (J. of Att. Dis. 2019; 23(1) 51-56)

Keywords

ADHD prospective memory executive function inhibition

Successful prospective memory (PM) performance is crucial to meet everyday social, occupational, and health-related demands (Kliegel, Jäger, Altgassen, & Shum, 2008). PM refers to the execution of delayed intentions at a certain time (time-based tasks) or event (event-based tasks; Einstein & McDaniel, 1996). Typical everyday examples of PM tasks are remembering to submit assignments on time or to pass a message to a friend when you see him next. Given the known deficits of individuals with ADHD with organizing and coordinating everyday activities, it is somewhat surprising that so far only four studies investigated PM in children and adults with ADHD (Altgassen, Kretschmer, & Kliegel, 2014; Brandimonte, Filippello, Coluccia, Altgassen, & Kliegel, 2011; Kerns & Price, 2001; Zinke et al., 2010). Kerns and Price (2001) presented children with ADHD with an event-based and a time-based task. For the event-based task, children were required to perform predefined activities during the course of the experiment (i.e., remembering to get up, go to the door and turn the doorknob when the experimenter snapped their fingers). Children with ADHD performed as well as controls. For the time-based PM task, children had to drive a car on a busy street (in a computer game) and remember to fuel the car at predefined times. Participants could monitor the remaining filling level by pressing a certain key. In comparison with controls, children with ADHD showed fewer correct time-based PM responses, while the total number of gas checks did not differ between groups. Using a standard experimental paradigm, Zinke et al. (2010) explored time-based PM performance in children with ADHD. Children were engaged in a one-back task and had to remember to press a specific button whenever 2 minutes had passed. Again, time-based PM performance was reduced in children with ADHD. Interestingly, groups did not differ in overall ongoing task performance or overall frequency and accuracy of time-monitoring. Brandimonte and colleagues (2011) explored event-based PM and response inhibition in children with autism and children with ADHD. Children worked on a categorization (ongoing) task and, simultaneously, either on an event-based PM (i.e., remembering to press a predefined button when one of two PM target cues was presented) or on a Go-/NoGo task (i.e., remembering not to press any buttons when one of two target items was presented). In comparison with matched controls, children with autism performed poorer in the PM task, while no group differences were observed in the Go-/NoGo task. In contrast, the opposite pattern of performance was reported for ADHD. Children with ADHD were as good as controls in the PM task, but showed reduced performance in the Go-/NoGo task. Altgassen and colleagues (2014) investigated both time- and event-based PM within one paradigm using parallel task constraints in the same sample of adults with ADHD. In line with previous research, a large-sized impairment was observed in adults with ADHD for time-based PM, while event-based PM was spared. Hence, taken together empirical evidence points to a task dissociation across PM task types in ADHD.

In terms of possible explanations for this dissociation, so far authors have mainly argued that, typically, time-based PM tasks are more demanding than event-based PM tasks and put higher demands on monitoring, inhibitory, and working memory load. Given that no external cue may prompt retrieval of the intended action, the individual needs to frequently inhibit performing the ongoing task to monitor the elapsing time and to keep the elapsed time in mind not to miss the target time (Einstein & McDaniel, 1996). Interestingly though, in all three studies, assessing time-based PM no group effects were found for time-monitoring (Altgassen et al., 2014; Kerns & Price, 2001; Zinke et al., 2010). Given that time-monitoring is considered the key marker for resource allocation in a time-based PM task (Kliegel, Martin, McDaniel, & Einstein, 2001), those results challenge the simple resource load explanation for the observed findings. Specifying this account, we recently suggested that for ADHD not time-monitoring per se, but rather the necessity to maintain the timing information in working memory, and/or to inhibit the ongoing task at target time execution may be potential underlying factors (Zinke et al., 2010).

Another potentially critical issue in previous studies on ADHD is that all event-based tasks used rather distinct or salient cues (e.g., finger snapping of the experimenter, Kerns & Price, 2001) or cues that were focal to the ongoing activity (Brandimonte et al., 2011). According to the multiprocess framework (McDaniel & Einstein, 2000), distinct, salient, or focal cues are assumed to enable rather automatic retrieval of the intended action and to put rather low demands on executive control processes. Given extensive evidence of reduced executive functioning (especially, inhibition) in ADHD (Barkley, 1997; Boonstra, Kooij, Oosterlaan, Sergeant, & Buitelaar, 2010), the use of tasks that imposed only minimal demands on executive control processes may have enabled participants to unimpaired performance in the previously used event-based PM tasks.

From a general clinical neuroscience view, condition-related spared or impaired PM performance may be mediated by a mismatch between PM task-specific requirements of cognitive resources (e.g., a PM task puts more or less demands on inhibitory control processes) and condition-specific impairments in those resources (e.g., a condition like ADHD may be associated with more or less available inhibitory resources; Kliegel, Altgassen, Hering, & Rose, 2011). In line with this reasoning reduced PM performance should only be expected, if the available resources are insufficient for the specific PM task (e.g., even individuals with generally reduced inhibition resources may have sufficient resources for a PM task with low inhibitory control demands). Applying this model to ADHD and the here-reported executive function deficit, PM impairments can be expected if the task puts high demands on executive (especially inhibitory) control. While spared PM performance may be expected in ADHD when executive control demands are low. Importantly, following the multiprocess framework (McDaniel & Einstein, 2000) not only time-based, but—depending on the specific task features—also event-based PM tasks may put high demands on executive control processes and self-initiated processing. A range of factors and dimensions have been suggested to determine the extent to which an event-based PM task invokes executive control processes. Of great importance is, for example, the relation of the prospective cue to the ongoing activity (i.e., its focality) and with this the similarity of the cognitive processes needed for performing the ongoing task and detecting the prospective cue. Furthermore, McDaniel and Einstein suggested that highly absorbing ongoing activities may lead to increased shielding of the currently active goal (ongoing tasks) and attenuated background monitoring for ongoing task-irrelevant, but potentially significant, stimuli (here, PM cues).

The goal of the present study was to systematically explore under which conditions event-based PM performance might be spared or impaired in adults with ADHD. Specifically, given previous evidence of reduced inhibitory control in ADHD (Barkley, 1997; Boonstra et al., 2010), the availability of inhibitory resources for performing the PM task was manipulated by asking participants to work on an acoustically presented task that put either low or high loads on inhibitory control processes, while performing at the same time an ongoing activity and an event-based PM task. Following our reasoning of higher executive control demands leading to PM deficits in ADHD, we expected adults with ADHD to show less correct PM responses than controls. Furthermore, we expected participants to show better PM performance when inhibitory control demands are low than when they are high. Moreover, we expected individuals with ADHD PM performance to differentially interact with inhibitory load: Individuals with ADHD were predicted to perform poorer than controls when inhibition load is high, but to show spared PM performance when inhibition load is low.

Method

Participants

In total, 36 adults participated in the present study: 18 individuals with ADHD (all men) and 18 healthy controls (17 men, 1 woman). Groups were equivalent for age (ADHD: M = 25.11, SD = 5.6, controls: M = 25.78, SD = 5.9; F < 1) and cognitive ability as indicated by the Matrix Reasoning test (ADHD: M = 10.89, SD = 2.8, controls: M = 10.44, SD = 2.1; F < 1). All participants spoke German as their first language. Diagnoses were established through expert clinical evaluation in accordance with Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; American Psychiatric Association, 2000) criteria: 4 adults were diagnosed with Attention Deficit Disorder and 14 with the Combined type. Individuals with ADHD were recruited through self-help groups and a local clinic. Controls were recruited through advertisements and the participants’ pool of the department. Twelve participants with ADHD were medically treated. Eight participants were on stimulants (e.g., Methylphenidate or Strattera), 3 took antidepressants, and 1 neuroleptic medication. Participants treated with stimulants were requested to refrain from taking medication 24 hr prior to testing. Exclusion criteria were any history of other psychiatric or neurological disorders as well as drug and alcohol abuse. Any human data included in this manuscript were obtained in compliance with the Helsinki Declaration. Each participant was tested individually and before testing, all participants gave written informed consent. Participants received 5EUR for their participation.

Materials

Cognitive functioning

General cognitive ability was measured by the Matrix reasoning of the Wechsler Adult Intelligence Scale–III (Wechsler, 1997; German version; Von Aster, Neubauer, & Horn, 2006). This test presented participants with a sequence of groups of designs, and the participant was asked to choose the missing design from a number of patterns. The test increased in difficulty. Raw scores were transformed into age-related normative scores.

PM Task—Following Altgassen, Kliegel, Rendell, Henry, and Zöllig (2008), a computer-based categorization task was used as the ongoing task. Three words per item were presented on a computer screen: one on top and two below. Participants had to decide as fast as possible which of the two words below belonged to the same category as the word presented above. They were required to indicate their answer by pressing a green key (which corresponded to the letter B on a personal computer [PC] keyboard) with the left index finger, if the left word matched the category or an orange key with the right index finger (which corresponded to the letter M on a PC keyboard), if the right word matched the category. The words were chosen from the Mannhaupt (1994) word norms and were part of the following categories: plants/nature, food/drinks, animals, people/human features, house/buildings, hobbies, devices/utensils. Each item was presented for 4 s and was followed by a 1-s interstimulus interval. Words were presented in front of a black background and their colors changed randomly from item to item (e.g., yellow, green, blue, orange, pink, red, or white). The dependent variable was proportion of correct responses.

For the event-based PM task, participants were instructed to press a pink key (which corresponded to the letter X on a PC keyboard), whenever the three ongoing task words were displayed in blue color (hence, non-focal PM cues were used). Participants were told that both the PM and the ongoing task were of equal importance. The dependent variable was proportion of correct responses.

The inhibition load task followed a procedure introduced by Bull, Phillips, and Conway (2008). Every 5 s, participants were presented with numbers ranging from 1 to 20 via headphones. Following a Go-/NoGo task paradigm, participants were told in the high inhibition load condition to add 3 to each presented number and say the result out loud, but to withhold saying the sum when it equaled 8 or 15. For the low inhibition load condition, participants were instructed to add 5 to every presented number and always say the result out loud. The dependent variable was proportion of correct responses.

Procedure

As for the order of testing, participants were first introduced to the inhibition load task (low or high inhibition load) and completed a single-task block (20 trials). Then, they were presented with the ongoing task, completed a single-task block of that task (20 trials), and were asked to perform the ongoing and the inhibition load task at the same time (dual-task block; either high or low inhibition load; 46 items each). Afterward, they were introduced to the PM task. After a filled delay, participants completed a triple-task block consisting of ongoing task (92 trials), PM task (4 items), and the respective inhibition load task (high or low inhibition load condition; 92 trials). This procedure was repeated (except for the introduction of the ongoing task) after a short break for the respective other inhibition load condition. Order of inhibition load condition was balanced.

Results

Mixed ANOVAs were conducted to analyze group (ADHD, controls; between-subjects factor) and inhibition load (high, low; within-subjects factor) effects on PM, ongoing task, and inhibition load task performance (see Table 1).

Table 1.

Prospective Memory, Ongoing Task, and Inhibition Load Task Performance.

	ADHD group M (SD)	Controls M (SD)	Group effect F ( df )	Inhibition load effect F (df)	Interaction effect F (df)
Prospective hits			4.29 (1, 34)*	.09 (1, 34)^a	.01 (1, 34)^b
Low inhibition load	.60 (.34)	.76 (.29)
High inhibition load	.63 (.30)	.78 (.28)
Ongoing task			19.53 (1, 34)***	15.19 (4, 136)***	2.13 (4, 136)^c
Single-task block	.88 (.09)	.97 (.05)
Dual-task block (low inhibition)	.81 (.15)	.96 (.03)
Dual-task block (high inhibition)	.77 (.19)	.94 (.06)
Triple-task block (low inhibition)	.75 (.13)	.89 (.06)
Triple-task block (high inhibition)	.75 (.17)	.91 (.05)
Inhibition load task			6.09 (1, 34)*	5.09 (5, 170)***	3.69 (5, 170)***
Single-task block (low inhibition)	.98 (.04)	.98 (.04)
Single-task block (high inhibition)	.96 (.04)	.98 (.04)
Dual-task block (low inhibition)	.95 (.06)	.99 (.02)
Dual-task block (high inhibition)	.92 (.12)	.96 (.04)
Triple-task block (low inhibition)	.92 (.10)	.98 (.02)
Triple-task block (high inhibition)	.89 (.11)	.98 (.02)

p < .05. ***p < .00. ^ap = .77. ^bp = .92. ^cp = .08.

Regarding PM performance, a significant group effect emerged from controls outperforming individuals with ADHD, F(1, 34) = 4.29; $η_{p}^{2}$ = .11. Neither the inhibition load $η_{p}^{2}$ = .003) nor the interaction effect was significant $η_{p}^{2}$ = .000).

With respect to ongoing task performance, a significant group, F(1, 34) = 19.53; $η_{p}^{2}$ = .37, and inhibition effect was found, F(4, 136) = 15.19; $η_{p}^{2}$ = .31. Overall, controls had more correct ongoing task responses, and both groups performed best in the single-ongoing-task block, followed by the dual-task block with low inhibition load, the dual-task block with high inhibition load and worst in both triple-task blocks. The interaction effect tended toward significance, F(4, 136) = 2.13; p = .08, $η_{p}^{2}$ = .06 (see Figure 1).

Figure 1.

Ongoing task performance across groups and blocks.

With regard to inhibition load task performance, significant group, F(1, 34) = 6.09, p < .05, $η_{p}^{2}$ = .15; inhibition load, F(5, 170) = 5.09, p < .001, $η_{p}^{2}$ = .13, and interaction effects, F(5, 170) = 3.69, p < .01, $η_{p}^{2}$ = .09, were found (see Table 1 and Figure 2). Overall, controls outperformed individuals with ADHD, and groups performed better in the single-task conditions and the dual-task condition with low inhibition load in comparison with the triple-task conditions and the dual-task condition with high inhibition load. Post hoc analyses point to significant group effects for the dual-task block with low inhibition load, F(1, 34) = 5.99, p < .05, $η_{p}^{2}$ = .15, and both triple-task blocks, low inhibition load: F(1, 34) = 5.63, p = .05, $η_{p}^{2}$ = .14; high inhibition load: F(1, 34) = 10.30, p < .01, $η_{p}^{2}$ = .23, with controls showing superior performance. For both single-task blocks, low inhibition load: F(1, 34) = .00, p > .05, $η_{p}^{2}$ = .00; high inhibition load: F(1, 34) = 1.55, p > .05, $η_{p}^{2}$ = .04, and the dual-task block with high inhibition load, no significant group effects were found, F(1, 34) = 1.84, p > .05, $η_{p}^{2}$ =.05.

Figure 2.

Inhibition load performance across groups and blocks.

Discussion

The goal of the present study was to explore the impact of inhibitory control processes on event-based PM performance in ADHD. To this end, we applied a procedure previously employed by Bull et al. (2008) and Klingberg and Roland (1997), which allows us to manipulate the availability of inhibitory resources in performing a target task; here, the PM task. Specifically, we asked participants to work on an ongoing activity into which an event-based PM task was embedded. In addition, as a third parallel task, they were required to work on an acoustically presented task that put either low or high loads on inhibitory control processes.

In line with our prediction that higher executive control load may lead to PM deficits in ADHD, individuals with ADHD showed reduced event-based PM when compared with controls. This is the first study to report a robust impairment of event-based PM in ADHD per se. As argued above, this seems to be in line with our conceptual model, predicting that deficits may more likely to emerge, if there is mismatch between PM task-specific requirements of cognitive resources and condition-specific impairments in those resources (Kliegel et al., 2011). The observed ADHD-related impairment in event-based PM may have been due to a non-focal PM task being used for the first time in the current study, which—according to the multiprocess model of PM (McDaniel & Einstein, 2000)—puts rather high demands on executive control processes (e.g., monitoring for the prospective cue). Moreover, the fact that participants had to simultaneously work on two other tasks (ongoing task plus inhibition task) could have contributed to the current findings because those additional tasks may have left participants with reduced cognitive resources (e.g., to monitor for the PM cue).

In contrast to our prediction of generally poorer PM performance when inhibition load was high as compared with low, we did not find any effects of inhibitory load on participants’ PM. Furthermore, there were no differential impacts of inhibitory load on event-based PM performance in ADHD. We had predicted ADHD individuals to show reduced PM performance when inhibition load is high and spared performance when inhibition load is low. However, across both inhibitory load conditions PM performance was reduced when compared with age- and cognitive ability-matched controls. Varying availability of inhibitory control resources did not affect PM performance. Importantly, ongoing task data clearly show that this is not due to the inhibitory task not being challenging enough as clear effects of the additional task emerged here. Together with previous studies that used this paradigm successfully to impose a general inhibitory load (Bull et al., 2008), these findings rather suggest an interesting conceptual conclusion; namely that it may not be necessary to have full inhibitory control available during the entire duration of an event-based PM task. Rather it may suffice to employ inhibitory processes after the PM cue has been detected and the ongoing task needs to be interrupted. As the paradigm imposed a rather tonic inhibitory load, in fact more phasic activation at cue detection may be required. Future studies will have to test this assumption, however.

With regard to participants’ performance in the inhibition load task, significant effects emerged from the factors group, inhibition load, and the interaction effect. Individuals with ADHD had less correct responses than controls (though both groups performed at ceiling). Importantly, inhibitory load and each additional task seem to have mainly affected individuals with ADHD. Individuals with ADHD showed most correct responses in the single-task block with low inhibition load and performance almost linearly decreased across the single-task block with high inhibition load, the dual-task and triple-task blocks (each with better performance under low than high inhibition load). In contrast, controls performed at a similar level across all conditions.

Taken together findings indicate reduced event-based PM performance in ADHD when general executive control loads are high. The present findings are limited by ceiling effects of both groups in the inhibition load task and ceiling effects in the ongoing task of controls. Future studies need to try replicate the findings using secondary tasks that are more difficult. A further limitation of the present study is the lack of severity data for ADHD symptoms. Moreover, future research should apply an extensive neuropsychological assessment to further describe potential differences between individuals with ADHD and controls and to explore possible underlying factors of PM performance in ADHD.

Footnotes

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) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The study was supported by SFB 940/1 2012.

Author Biographies

Mareike Altgassen graduated from the University of Heidelberg, Germany, in 2004. She completed her PhD in 2007 at the University of Zurich, Switzerland. She then worked as an assistant professor at the Technische Universität Dresden, Germany. Since 2012, she has also been employed as an assistant professor at the Donders Institute for Brain, Cognition and Behaviour Centre for Cognition at the Radboud University Nijmegen, The Netherlands.

Andrea Koch studied psychology at Technische Universitaet Dresden, Germany. After a research internship at the Austin Repatriation Hospital in Melbourne, she graduated in 2012. She is now doing her PhD in a multicenter research project at the University Hospital Carl Gustav Carus in Dresden.

Matthias Kliegel graduated from the University of Mainz, Germany, in 1999 and completed his PhD at the University of Heidelberg, Germany, in 2002. He then worked as an assistant professor at the University of Zurich, Switzerland, before he was appointed full professor at the Technische Universitaet Dresden in 2007. Since fall 2011, he has been a full professor at the University of Geneva in Switzerland.

References

Altgassen

Kliegel

Rendell

P. G.

Henry

J. D.

Zöllig

. (2008). Prospective memory in schizophrenia: The impact of varying retrospective-memory load. Journal of Clinical and Experimental Neuropsychology, 30, 777-788.

Altgassen

Kretschmer

Kliegel

. (2014). Task dissociation in prospective memory performance in individuals with ADHD. Journal of Attention Disorders, 18, 617-624.

American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington, DC: Author.

Barkley

R. A

. (1997). Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD. Psychological Bulletin, 121, 65-94.

Boonstra

A. M.

Kooij

J. J.

Oosterlaan

Sergeant

J. A.

Buitelaar

J. K

. (2010). To act or not to act, that’s the problem: Primarily inhibition difficulties in adult ADHD. Neuropsychology, 24, 209-221.

Brandimonte

M. A.

Filippello

Coluccia

Altgassen

Kliegel

. (2011). To do or not to do? Prospective memory versus response inhibition in autism spectrum disorder and attention-deficit/hyperactivity disorder. Memory, 19, 56-66.

Bull

Phillips

L. H.

Conway

C. A

. (2008). The role of control functions in mentalizing: Dual-task studies of theory of mind and executive function. Cognition, 107, 663-672.

Einstein

G. O.

McDaniel

M. A

. (1996). Retrieval processes in prospective memory: Theoretical approaches and some new findings. In Brandimonte

M. A.

Einstein

G. O.

McDaniel

M. A

. (Eds.), Prospective memory: Theory and applications (pp. 115-142). Mahwah, NJ: Lawrence Erlbaum.

Kerns

K. A.

Price

K. J

. (2001). An investigation of prospective memory in children with ADHD. Child Neuropsychology, 7, 162-171.

10.

Kliegel

Altgassen

Hering

Rose

N. S

. (2011). A process-model based approach to prospective memory impairment in Parkinson’s disease. Neuropsychologia, 49, 2166-2177.

11.

Kliegel

Jäger

Altgassen

Shum

. (2008). Clinical neuropsychology of prospective memory. In Kliegel

McDaniel

M. A.

Einstein

G. O

. (Eds.), Prospective memory: Cognitive, neuroscience, developmental, and applied perspectives (pp. 283-308). Mahwah, NJ: Lawrence Erlbaum.

12.

Kliegel

Martin

McDaniel

M. A.

Einstein

G. O

. (2001). Varying the importance of a prospective memory task: Differential effects across time- and event-based prospective memory. Memory, 9, 1-11.

13.

Klingberg

Roland

P. E

. (1997). Interference between two concurrent tasks is associated with activation of overlapping fields in the cortex [Research Support, Non-U.S. Gov’t]. Cognitive Brain Research, 6, 1-8.

14.

Mannhaupt

H.-R

. (1994). Produktionsnormen für verbale Reaktionen zu 40 geläufigen Kategorien [Production norms for verbal reactions to 40 familiar categories]. In Hager

Hasselhorn

. (Eds.), Handbuch deutschsprachiger Wortnormen [Handbook of German word norms] (pp. 86-101). Göttingen, Germany: Hogrefe.

15.

McDaniel

M. A.

Einstein

G. O

. (2000). Strategic and automatic processes in prospective memory retrieval: A multiprocess framework. Applied Cognitive Psychology, 14, S127-S144.

16.

Von Aster

M. G.

Neubauer

Horn

. (2006). Wechsler Intelligenztest für Erwachsene - WIE [Wechsler Adult Intelligence Scale]. Frankfurt, Germany: Harcourt.

17.

Wechsler

. (1997). Wechsler Adult Intelligence Scale (3rd ed.). San Antonio, TX: Psychological Corporation.

18.

Zinke

Altgassen

Mackinlay

R. J.

Rizzo

Drechsler

Kliegel

. (2010). Time-based prospective memory performance and time-monitoring in children with ADHD. Child Neuropsychology, 16, 338-349.