Introduction
For the fact that a dysfunction of the executive system in Autism Spectrum Disorder (ASD) is one of the main accounts for the primary symptoms of this condition (Russel, 1997) a considerable large amount of research have been devoted over the last decades to the study of the executive system functioning in ASD. This proposal might be best in explaining a core diagnostic feature in ASD—the presence of repetitive behaviors and restricted interests (Hill, 2004). Autism, is a developmental disorder marked by the presence of at least one core symptom in three different domains: social interaction; communication and repetitive behaviors and restricted activities (see for instance Wadhera and Kakkar, 2019). The recent edition of Diagnostic and Statistical Manual of Mental Disorder (DSM—5th edition) have combined different diagnostic labels (e.g., Asperger syndrome or Autism disorder) under a single umbrella term “ASD” stressing the idea of a spectrum of deficits on the different domains (Wadhera and Kakkar, 2019).
The executive system, at use for adaptive responses to novel or complex situations, encompasses many distinct and diverse functions from planning and working memory to inhibition and mental flexibility but also initiation of a response, all of which are primarily attributed to the frontal lobes (Stuss, 1992). Yet it is accepted now that autistic individuals might not encounter problems across all executive domains (Geurts et al., 2004). Importantly, however, is the fact that the majority of tasks designed to measure executive functions depend on non-executive functions, as perception or memory, and also problematic is the fact that each task is never a pure measure of a single executive domain (Pennington and Ozonoff, 1996; Geurts et al., 2004).
Several studies addressed and have evaluated the pattern of preserved vs. spared functioning of distinct executive domains in ASD. However, the picture is not simple and not always consistent. One of the seminal works by Ozonoff and Jensen (1999) evaluated both cognitive flexibility and planning (with the Tower of Hanoi) and found these domains to be impaired in their sample. The same sample of autistic children show, however, a preservation of inhibition of a response (in the Stoop test) (Ozonoff and Jensen, 1999). Another multi-task study that also included the Stroop test and the Tower of Hanoi, reported preserved functioning of inhibition and planning, respectively, and also preserved functioning of cognitive flexibility, with only the working memory domain being compromised (Goldberg et al., 2005). A different approach is used in other studies where, for a given executive domain more than one task was considered. In Geurts et al. (2004) several tasks were applied aiming to evaluate the contributions to planning, working memory, flexibility, fluency and inhibition and found that all but the working memory component were compromised. In the same line, another study included a battery of seven different tasks aiming at evaluating their contribution to planning/working memory, flexibility and response inhibition. In this study, with children and adolescents, it was reported, from their composite scores, a poor performance of the ASD sample on inhibition and planning/working memory but not on cognitive flexibility (Happé et al., 2006). In this study, it was also compared the different profiles in young vs. old participants and results show that the differences observed were only present for the younger group. Authors concluded that this age-related improvements are indicative that executive functioning deficits may ameliorate with increasing age (Happé et al., 2006). A study focused on eye movement responses evaluated different executive domains from infancy to adulthood as they aimed to assess delayed or impaired development (Luna et al., 2007). They evaluated response initiation, response inhibition and working memory components, and found, overall, troubles in all domains. The autistic participants were slower in the latency to initiate memory guided saccades, but this finding was only present in adult participants. In response inhibition and working memory there was overall a poor performance, but both the ASD and control samples showed developmental improvements, yet with differences in the stabilization/adult level response (Luna et al., 2007). A 10-year longitudinal study evaluated the trajectories of executive functions from childhood into adulthood, with a 2- and 10-years follow ups (Fossum et al., 2021). This study focused on working memory component, inhibition (Color-Word interference test) and on planning abilities, and revealed that at baseline (12 years old in average) the ASD sample had a poorer performance than the control sample, on all domains. Importantly, they found that although the performance gap was not reduced along time, the maturation slopes were similar across groups, which led the authors to concluded that their results support the hypothesis of a similar rather than diverging developmental trajectories (Fossum et al., 2021).
The diversity and complexity of tasks and the different approaches used on studying executive functioning in ASD makes it difficult for a clear or overarching account, however, at least two review studies concur on the existence of deficits in both cognitive flexibility and planning (Pennington and Ozonoff, 1996; Hill, 2004). A recent review study concurs also on the existence of deficits in cognitive flexibility (but not on planning) and found also support for deficits on the working memory component (St. John et al., 2022), which were also reported in the Pennington and Ozonoff (1996) review. Regarding inhibitory control, these review studies reported either that findings were rather inconclusive (St. John et al., 2022) or that inhibition of a response in this population was unimpaired for neutral responses or inhibitory deficit per se, but that autistic individuals might be moderately impaired, or impaired in certain cases, in inhibiting prepotent responses (Pennington and Ozonoff, 1996; Hill, 2004).
Several studies have been devoted to the study of inhibitory processes in ASD and it has been acknowledged the importance of using multiple measures to evaluate a single cognitive construct (Christ et al., 2007). Inhibition is a component of the executive system that allows individuals to withhold prepotent responses or ignore distracting stimuli (Adams and Jarrold, 2012), for which individuals must suppress the activation or processing of information that would otherwise interfere with the achievement of a cognitive or behavioral goal (Dempster, 1992). The main tasks used to assess inhibitory control are the Stroop test, the Go/no-go task and also the Flankers task, where the firsts are considered measures of prepotent response inhibition and whereas the latter is a task of resistance to distractor interference (Adams and Jarrold, 2012).
In ASD it has been proposed that individuals might encounter troubles in some aspects of the inhibitory control but not all. Specifically, it has been proposed that autistic individuals have a selective deficit with an impaired ability when needing to ignore distracting information but preserved inhibition of prepotent responses (Christ et al., 2011). In accordance, it has been shown in quite a few studies that the performance of ASD children is unimpaired in Stroop tasks (Ozonoff and Jensen, 1999; Goldberg et al., 2005; Christ et al., 2007). Also in a tasks analogous to the Stroop test (e.g., the D-KEFS word interference task) it was reported that both in children and adults the performance is preserved (Christ et al., 2011; Mostert-Kerckhoffs et al., 2015, but see Corbett et al., 2009 for contrasting results in children). Along the same line, it has been generally found a preserved performance in a Go/no go task (or in an analogous Stop-signal task), where the performance of children seems to be preserved (Ozonoff and Strayer, 1997; Happé et al., 2006; Christ et al., 2007; Adams and Jarrold, 2012), which, however, contrasts with recent findings of Wilson et al. (2014) in adults, and in children by Schmitt et al. (2019). Regarding the Flankers task, the pattern is the opposite with the majority of studies reporting that ASD children have considerable difficulties with this type of tasks (Christ et al., 2007, 2011; Adams and Jarrold, 2012, but see Ozonoff and Strayer (1997) that reported preserved performance in children in a distractor task). Notwithstanding, results of a meta-analysis regarding inhibitory control in ASD show that both prepotent response inhibition and resistance to distractor interference were found to be deficient in ASD individuals, and strikingly with a larger effect for measures of prepotent inhibition which seems to be more difficult for ASD individuals than interference control (Geurts et al., 2014). Moreover, in a meta-analysis of imaging studies it was found, for adult participants, a difference in convergence in the right inferior frontal gyrus when contrasting with control samples, when performing inhibitory tasks. When comparing autistic adults with a younger sample a divergence of convergence on the left inferior frontal gyris was observed. These findings indicate that these areas are likely to be recruited to solve inhibition tasks in autistic adults, but that abnormalities are not evident until adulthood (Zhang et al., 2020).
For studying response inhibition another task, a sentence-completion one, has been used. The Hayling test constructed by Burgess and Shallice (1996) allows the direct comparison between response inhibition and response initiation, with minimal changes across conditions. The idea that both these processes are subserved by similar and overlapping functional systems have been tested and demonstrated (Burgess and Shallice, 1996; Nathaniel-Jones et al., 1997). Importantly is the fact that, in any inhibition tasks, such as the Stroop test, the inability to suppress the most salient response is related to the ability or not to initiate a response (see Burgess and Shallice, 1996). In the Hayling test, sentences are presented to the participant with the last word omitted (e.g., “Most sharks attack very close to the ________”). All sentences, randomly assigned to either Part A—response initiation or Part B—response inhibition, have a very high probability of a particular response. In Part A, in the one hand, participants are asked to provide an ending that makes sense (obvious response) and that fits the sentence context. On the other hand, in Part B participants must provide an ending word which makes no sense in the context of the sentence, hence the high-probability ending word must first be suppressed (Burgess and Shallice, 1996). Error scores and latencies can be analyzed. These authors propose also a score in which the latencies of Part A are subtracted from Part B (B-A latencies) in order to remove the confound factor of initiation problems when considering the latencies in the response suppression condition (Burgess and Shallice, 1996).
A handful of studies have used the Hayling test in Autism, both in adults (Boucher et al., 2005; Hill and Bird, 2006; Johnson et al., 2011) and in children (Robinson et al., 2009), reporting conflicting results. If in the one hand, the Haying test performance in autistic children seem to lead to significant differences, both in error scores and in response times in the inhibition condition but not in part A (Robinson et al., 2009). Also, in the seminal work of Boucher et al. (2005) on the Hayling test with adolescents and adults, in which only error score were reported, differences for the inhibition—Part B condition were observed, with an increased number of errors for the ASD sample as compared to the control group. On the other hand, the work of Hill and Bird (2006) and Johnson et al. (2011) showed no error score differences for neither Part A nor Part B. These two studies, with adult participants, did, however, analyzed the response latencies of both conditions and found overall that the autistic participants took longer than their control samples when performing both Part A and Part B. Neither of these two studies have reported the B-A latencies differences.
In contrast to response inhibition, or other executive functions, the initiation of a response in ASD is likely the less studied executive domain, despite of its importance to a host of behaviors. Two recent reports based on first-hand accounts from people on the spectrum have stressed the importance of this executive function on their condition perception. Welch et al. (2019) study gives some hints regarding the perceived mismatch between what is seen on the outside (i.e., behaviors; e.g., not making eye contact) and what is going on in the inside (i.e., intentions; e.g., interest in social contact) (Welch et al., 2019). Along the same line, Buckle et al. (2021) studied inertia—the inability in acting on the intentions—with focus groups and first-hand accounts from adults with ASD. An overarching theme found in this study was the difficulty in initiating tasks of any type, even simple ones. Scaffolding to support action was also a consistent theme found, with prompting from the external environment leading to promoting actions in this population (Buckle et al., 2021). In an experimental setting, Carmo et al. (2015, 2017) have analyzed the performance in a verbal fluency task as function of time in adults with ASD, and observed that in the first time period this group of participants produced fewer words as compared to the control group but that in the remaining time periods the differences between groups were no longer present. These authors considered that this pattern of results could signal a deficit at the initiation of the task, and have also showed that with a simple external verbal cue the deficit was no longer observable (Carmo et al., 2017).
With the current study we aim at further investigating both initiation and inhibition processes in ASD, in a single sentence-completion task with minimal changes across conditions and interchangeable stimuli (adapted from the Hayling test and extended). High-functioning adult participants diagnosed with ASD and an age-, gender-, schooling- and general cognitive abilities- matched control sample performed this sentence-completion task, with two conditions: response initiation (Part A) and response inhibition (Part B). Critically, we evaluated in ASD the contribution of possible initiation difficulties to the overall inhibition (Part B) response times by analyzing the B-A latencies, as proposed by Burgess and Shallice (1996). As mentioned before, each task is never a pure measure of single component of the executive system, and initiation of a response is particularly pervasive to a multitude of functions and behaviors, and have been considerably neglected. If it is the case that initiation of a response processes are impaired in this population, we anticipate that when correcting for this confound effect, the putative inhibitory difficulties in ASD might no longer be observable.
Discussion
In our study we aimed at disentangling the contribution of initiation processes difficulties in autism from putative difficulties in inhibitory processes in this population. Adult participants with high-functioning autism and a well-matched control sample performed a sentence-completion task, with minimal changes across conditions and interchangeable stimuli, similar to the Hayling test (see Burgess and Shallice, 1996). This task comprised two different conditions, presented in a fixed order, in which Part A engaged processes regarding the initiation of a response, whereas in Part B, participants were required to inhibit a prepotent response (Burgess and Shallice, 1996). Critically we analyzed the B-A latencies—subtraction of participants’ response times of Part A from the response times of part B—as proposed by Burgess and Shallice (1996) for the evaluation of the impact of response initiation difficulties, which have been reported in ASD, on response inhibition abilities.
Foremost, our results on the performance of Part A show that already in this task condition participants with ASD were considerably slower than their control group (ASD: M = 2432.5; Controls M = 1078.5). This result is in line with the results obtain in a verbal fluency task, where differences in performance were observed in participants with ASD in the first time bin analyzed, whereas in the remaining of the task the differences between them and the control group were no longer present (Carmo et al., 2015, 2017). These results were interpreted by the authors as indicative of troubles at the initiation of a response in autism, which is corroborated by the present findings. The hypothesis of an impairment in response initiation in ASD has received recent reinforcement by first-hand accounts from individuals with ASD, in which a common theme disclosed was the difficulty in initiating tasks of any type (Buckle et al., 2021). Critically to this issue, is the fact that external environmental prompting have been reported, either experimentally or from first-hand accounts, to ameliorate initiation difficulties in this population (Carmo et al., 2017; Buckle et al., 2021), which is of great importance to change implementations in practice. This prompting aid could, for instance, be easily implemented in professional settings, where a supervisor could provide some external cues in the beginning of each task, and hence facilitate the difficulties in task initiation. Besides this external cues aiding, the fact that the latencies in initiation of a response increase the overall time of execution, it could be implemented, for instance in educational settings, an adjustment in terms of the amount of time allowed to complete a given task (e.g., extra time for an exam). Considering that the initiation of a response is needed for possibly all kind of overt behaviors, this line of research is quite auspicious and deserving of attention in future studies, ultimately seeking changes in applied settings that could significantly impact the daily lives of those with this condition.
Results regarding performance scores on both task conditions (entropy and accuracy measures) show no observable differences between the two groups (ps > 0.17) with very low entropy and very low amount of errors, respectively, and are as such, in line with the results of both Hill and Bird (2006) and Johnson et al. (2011), disconfirming as well the results reported by Boucher et al. (2005) in their seminal work with the Hayling test in adolescents and adults with ASD (see Table 3 for a better comparison with relevant literature).
At a first glance our results on response times would indicate that adults with ASD indeed struggle with inhibitory processes (ASD M = 6758.3 ms; Controls M = 3283.9 ms), as it have been proposed in the literature (e.g., Geurts et al., 2014). Our findings on reaction times are also consistent with findings of the Hayling test on adult population (see Table 3). Even if in our sample, participants with ASD were perfectly able to suppress the prepotent response and were able provide a correct response, with comparable strategy use, they might have needed additional processing time to do so. Yet when considering the B-A latencies results, we show that the differences observed for part B (Inhibition condition) were no longer observed (ASD: M = 4325.76 ms; Controls: M = 2205.46 ms). In this analysis, proposed by Burgess and Shallice (1996) in order to eliminate the confound effect of response initiation difficulties, we subtracted from the average response times in Part B, the average response times in the initiation condition (Part A), and our results indicate that indeed no differences between the ASD and control groups might be attributable to inhibition processes, but rather to difficulties in the initiation of a response. This result is quite important and questions the deficits reported not only in studies with the Hayling tests (e.g., Hill and Bird, 2006; Johnson et al., 2011), but with all sorts of tasks targeting inhibitory processes in autism, in particular tasks requiring the suppression of a prepotent response (e.g., Wilson et al., 2014; Schmitt et al., 2019, for Go/no Go tasks). Highlighting the importance of taking into account this somehow neglected executive function when evaluating cognitive hypothesis in ASD, for its pervasive impact on virtually all overt behaviors and cognitive domains. Regarding, particularly, studies of inhibitory processes in autism (but not exclusively), a component of the executive function that have been proposed to be impaired in this population, it would be strongly recommended to design future studies that are able to account for or to remove the impact of response initiation delays in ASD, which have now received some additional empirical support.
The current study evaluated initiation of a response and inhibition abilities of adult participants exclusively, and we advise against any generalization to younger autistic population. Results on age and development regarding executive functions in autism, namely on inhibitory processes, are quite discrepant, with impairment being observed in children only, ameliorating with increasing age (Happé et al., 2006), or present both in children and adult samples (Fossum et al., 2021), or that brain abnormalities are observable in adults only (Zhang et al., 2020). Likely developmental differences, and the time course of maturation of the frontal lobes, are the reasons for what we consider generalizations are to be avoided when studying any executive function. Regarding processes of response initiation our results would be consistent with existent studies on this executive function, that reported, for instance, troubles on initiation in adult samples only (Luna et al., 2007), or children’s preserved performance on the Hayling test (see Table 3). Note, however, that this does not mean that generalization should be carried out, and that only with further developmental studies on response initiation we will be able to understand whether initiation impairments are really only observable later in development.
At last, some limitations of the current work, and a summary of main recommendations should be mention. In the first place, our sample size is relatively small which makes, particularly, the results on the accuracy measures, which were found non-significant, of deserving further evaluation with a considerably larger sample, and to be taken with cautious. Secondly, we have tested a sample of adults participants only, for what results should not be generalized to other age groups. We found this developmental aspect of particular interest given the results on the Hayling test reported for younger samples. As already mention, it would be important to understand whether impairments reported regarding response initiation in autism are really only present or observable in adult populations or if they appear early in development.
As further recommendation we would like to add that general results on inhibitory control in ASD, or on other executive domains, might be impacted by response initiation deficits and further direct evaluation would be critical. Moreover, our study does not address the potential beneficial impact of external cues or prompting on response initiation. The fact that this mitigation of response initiation difficulties is of great importance and could impact the daily life of autistic individuals, it should definitely deserve further and pressing attention.
In sum, we have shown that when removing initiation of a response delays in participants with ASD, differences regarding inhibitory processes are no longer observed, questioning the reported deficits of this executive function in autism. We offer, as well, additional support for the hypothesis of an impairment of processes of response initiation in autism, a function that is likely involved in a multitude of behaviors and cognitive domains and that should deserve cautious and careful attention when designing future studies on autism. The importance of studying the initiation of a response also reflects the fact these deficits that have been shown to ameliorate by external prompting, which could lead to changes in practical setting, with a considerable impact on the lives of those with autism.