There appear to be both strengths and weaknesses to decreased sensory gating, one of the neurophysiological measures thought to reflect the brain's early filtering mechanism of incoming environmental information to reduce strain on higher brain functions (1). On the one hand, reduced filtering may cause more distractibility and errors due to the flooding of higher brain functions with unnecessary information (2, 3). Hence, overloading the higher order cognitive system, this higher influx of information from the environment could result in attentional problems. Micoulaud-Franchi et al. (4) showed that the experience of being flooded with sensory stimuli that is often reported by individuals with ADHD could be explained by reduced sensory gating, which strengthens previous reports on this topic (5). On the other hand, it can be beneficial during a situation in which there are several courses of action necessary or during creative acts, by giving an individual more information to choose from Carson et al. (6), Gonzalez-Carpio et al. (7), and Zabelina et al. (8). A common definition of creativity is that it is the interaction between process, ability, and environment to create something meaningful and original based on contextual factors (9, 10). Since the benefits of promoting creativity in primary school curricula are increasingly accepted and implemented (11, 12) while in turn creativity has been linked to attentional difficulties (13) the current paper investigated sensory and sensorimotor gating in relation to creativity and attention. Distractibility and inattention are often thought of in a negative connotation due to the social and reward structures that are in place in current western societies (roughly 60% of the general population is thought to have at least one symptom of hyperactivity or inattention) (14), leading to stigma and lower quality of life in those with an attentional disorder (15, 16). The current study aimed to investigate whether there are also benefits to such attentional profiles that are associated to a higher influx of sensory stimuli due to reduced sensory and/or sensorimotor gating.

Two paradigms commonly believed to measure the early, pre-conscious filtering of irrelevant or distracting information are sensorimotor gating (prepulse inhibition of the startle reflex, or PPI) and sensory gating (P50 suppression). During PPI, a muted or inhibited magnitude of the startle reflex is observed when an intense, startle eliciting stimulus is presented after a weak stimulus (the prepulse). In humans, this is usually assessed with electromyography (EMG) of the orbicularis oculi muscle (17–19).

Similar to PPI, P50 suppression represents the influence of inhibitory processes triggered by earlier presented stimuli. In a typical P50 paradigm, participants are presented pairs of identical auditory stimuli with an ISI of 500 ms (8, 20). In healthy participants, the event related potentials (ERPs) to the second stimulus are usually reduced, starting from the positivity emerging in the electroencephalogram (EEG) after 50 ms (P50) onwards (21–23). This decrease in P50 amplitude is thought to reflect sensory gating.

Some studies report that P50 suppression and behavioral attentional measures are positively correlated (24–26), but studies showing that measures of attention and P50 suppression are unrelated also exist (27, 28). This discrepancy is likely due to the different attentional measures that were assessed in these studies. In children (age 9–14), symptomatology of the attentional disorder ADHD has been negatively associated with levels of P50 suppression, as well as its peak amplitude, and peak latency (29). Likewise, a study with adults reported that individuals with ADHD had lower average P50 suppression compared to healthy controls (30). However, others report that P50 deficits are not associated to disorders that are related to a wider distribution of attention such as ADHD or first-episode psychosis (31, 32). Similar to P50 suppression, children with ADHD have been shown to have reduced levels of PPI (33). Yet, results are scarce and do not show a definite relation given that replications of this result in adults and in adolescents were unsuccessful (30, 34, 35). Moreover, while the majority of studies have shown that gating deficits are unrelated to neuropsychological measures (30, 32, 34, 36), there are some interesting exceptions. For instance, a positive association between executive functioning and P50 suppression has been reported in patients with schizophrenia (37) and Alzheimer's disease (38). There are also reports on positive associations between executive functions and PPI (39–41). Executive functions are a neuropsychological concept that is commonly defined as those higher order cognitive functions that are important for planning and reaching one's goals (42) and have for instance been shown to be important in the performance of creative tasks (43, 44). These studies indicate that even though often left uninvestigated, sensory gating can be seen as the preliminary filtering system, before executive functions, that plays a role in creative cognition (45). There are accounts that indicate that when the environment is rich in stimuli and contains many action possibilities, this might lead to more creative ideations. That is, if individuals are able to perceive many action possibilities due to reduced sensory gating, even if these possibilities are only implicitly relevant to the task at hand, they are able to use that knowledge creatively. Additionally, less stringent filtering processes might also lead to an influx of less relevant knowledge into working memory when working on a task (46–48). Hypothetically, when more leaky attention (for instance due to reduced sensory gating) is present, chances increase that more (implicitly relevant) action possibilities will be observed and used during creative tasks. Taken together, these reports suggest that less stringent gating abilities lead to increased creativity by exerting influence on executive functions.

To date, only two EEG-studies exist in which the association between sensory gating and creativity was investigated (8, 49). Zabelina et al. reported that divergent thinking was related to increased sensory gating and that real-life creative achievements were related to reduced sensory gating in a sample of healthy adults (8). They therefore reasoned that divergent thinking depends on the ability to rapidly focus attention by restraining sensory gating. However, results may be different when there are no severe time constraints. Since reduced gating theoretically leads to a wider range of available stimuli in working memory to combine, this in turn might increase the amount of creative ideations that are generated (50, 51). This is in line with the second study that examined P50 suppression in relation to divergent and convergent measures of creativity (49). They found that while convergent thinking was positively related to reduced sensory gating, there was a negative association between the divergent thinking measure fluency and sensory gating. In addition, no relation was found with the divergent thinking measure of originality.

Thus far, not much creativity research exists that makes use of neuroscientific methods. By investigating these underlying mechanisms of behavioral concepts such as attention these methods can contribute to valuable new insights of such concepts. As such, it is increasingly accepted that a continued effort should be made to increase our knowledge by providing a more mechanistic account of processes such as attention and creativity (52, 53). Neurocognitive disorders related to attentional deficits such as schizophrenia and ADHD have been associated with both sensory gating deficits and increased creativity (54, 55). However, results also suggest that as symptom severity increases to clinical levels, potential strengths such as being more creative often disappear (54, 56, 57). Therefore, the current study aims to investigate if individual differences in sensory and sensorimotor gating that are present in the general population can explain the relationship between attention and attentional deficits such as those found in ADHD and creative thinking.

We hypothesized that higher levels of creativity as well as attentional difficulties would be related to an individual's increased responses to irrelevant stimuli, and thus lesser PPI and P50 suppression. Additionally, we exploratively examined if there was a difference in sensory- and sensorimotor gating between those children in our population that happened to have an ADHD/ADD diagnosis and typically developing children.

All tests were performed at the Utrecht Medical Centre in The Netherlands and approved by the Faculty Ethics Review Board (FETC18-081) of the Faculty of Social and Behavioural Sciences at Utrecht University and the Medical Ethical Committee of the Utrecht Medical Centre (NWMO18-849).

Table 1 shows the descriptive statistics of the P50 suppression parameters, creativity, and attentional outcome measures. Table 2 shows descriptive statistics of the PPI parameters, creativity, and attentional outcome measures. The correlation matrix (see Supplementary Table 1) shows all measures that were correlated in the current study. Based on the significant correlations displayed there, we corrected for intelligence on all creativity measures. Furthermore, we corrected for gender on PPI trial types PPI 7660, PPI 8560, and PPI 85120. Based on the scatterplots between the main variables of the current study (see Supplementary Figures 1, 2) we removed two additional participants from further analyses related to the PPI parameter PPI 7660 due to extreme values (value −158 and value −2,232).

Based on our hypothesis that the low sensory gating group would have increased creativity scores we first performed multiple regression analyses to assess the relation between the psychophysiological measures, creativity and attention, but found no significant associations between these measures, likely due to our sample size (see Supplementary Table 2 for the P50 suppression parameters and Supplementary Table 3 for the PPI parameters). To explore possible associations between these measures more thoroughly, we subsequently split the participants on the sensori(motor) gating parameters and performed ANCOVAs to test our predictions. These results can be viewed in Table 3. When split on (above and below) average conditioning amplitude we found no significant group effects on any of the creativity scores, i.e., fluency, flexibility, originality, or TCTDP. When split on (above and below) average testing amplitude a significant main effect of group was found on fluency and flexibility, indicating higher creativity scores in the group with higher testing amplitude than in the group with lower amplitudes. These significant associations are depicted in Figure 1. However, no significant main group effect was found on originality or TCTDP. Similar to the split on conditioning amplitude, when split on (above and below) average T/C ratio no significant group effects in the creativity measures were found for fluency, flexibility, originality, or TCTDP.

Since the SDQ attention scale did not significantly correlate with any of our covariates, Mann Whitney U tests were performed to test our prediction that the group with low sensory gating would have increased attentional difficulties. These tests showed no significant group differences when groups were split on (above or below) average conditioning amplitude (U = 414.50, p = 0.617), testing amplitude (U = 32.13, p = 0.727), or T/C ratio (U = 376, p = 0.414).

Correlational analyses between P50 measures and measures of creativity and the SDQ attention scale showed only one significant correlation: the conditioning amplitude correlated significantly positive with flexibility (r_s = 0.338, p = 0.007).

Next, we spilt groups above or below average PPI to test our predictions. Results can be viewed in Table 4. No significant group differences were found for any of the creativity outcome measures (i.e., fluency, flexibility, or originality, or TCTDP) when group were split on above or below average PPI parameters pulse alone amplitude, PPI 7660, PPI 76120, PPI 8560, or PPI 85120. In addition, no significant group differences were found in the SDQ attention scale when groups were split on pulse alone amplitude, PPI 7660, PPI 76120, PPI 8560, or PPI 85120 and neither did any of the PPI measures correlate significantly with any of the creativity or attentional measures (r_s < −0.238, p = 0.156).

To inspect if children with (a suspicion of) ADHD/ADD differed in their P50 suppression or PPI in comparison to children without ADHD/ADD we performed Mann Whitney U tests. Descriptive statistics for the ADHD/ADD group and non-ADHD/ADD group are displayed in Table 5. These tests showed no significant group differences on the conditioning amplitude (U = 147.5, p = 0.289), testing amplitude (U = 188, p = 0.861) or T/C ratio (U = 166.5, p = 0.517), PPI 7660 condition (U = 49.00, p = 0.220), PPI 76120 condition (U = 152.5, p = 0.535), PPI 8560 condition (U = 162.5, p = 0.702), or the PPI 85120 condition (U = 157.5, p = 0.616).

The current study found that children with a higher P50 amplitude in response to testing stimuli in the P50 suppression paradigm had significantly higher scores on the creative measures of fluency and flexibility. No other significant differences between high and low scoring children on any of the remaining measures of sensory- or sensorimotor gating were found on other creativity measures, scores on attentional difficulties, or having an ADHD diagnosis or not.

Contrary to a previous report on a healthy adult sample that found higher creativity scores related to higher sensory gating as measured by the T/C ratio (8), we found that the children in our study with above group average responses to testing stimuli of the P50 suppression paradigm scored higher on creative fluency and flexibility (however, please note that no significant differences were observed for the T/C ratio or conditioning amplitude). Zabelina et al. (8) attributed their result to the 3 min time constraint and emphasize on the quantity of responses during their divergent thinking task. Perhaps this increased the focus on timing, resulting in less creative quality of responses (69). In comparison, the time limit of the divergent thinking task in our study was 25 minutes, which may have led to benefits of a reduced capacity for sensory gating. Alternatively, the differences between the results could also be explained by the fact that Zabelina et al. (8) reported on healthy adults, while we report on a naturalistic sample of primary school children.

We found no evidence for an association between increased originality and reduced sensory gating. It is likely that participants who experience less bottom-up control will think of more answers because such a state of dispersed attention facilitates idea generation (70). Likewise, the conditioning P50 amplitude has been reported to negatively relate to verbal fluency before (36), indicating that individuals who respond more intensely to conditioning stimuli score higher on verbal fluency when confronted with distractions. Hence, distracting, seemingly irrelevant stimuli may contain relevant information for tasks that require multiple solutions. In comparison, originality is more akin to convergent processes because it is based on finding a solution that is most optimal or novel (71). This process is different from the quantitative nature of fluency and flexibility. The ability to produce many or different responses may indeed benefit from attenuated sensory and sensorimotor gating because it is related to the preparation and incubation stage of creativity, which focusses on idea generation and assessing all possibilities (72). The second two stages are more convergent; assessment of ideas takes place whereafter the optimal response is selected. When selecting the most novel and original response, quality assessment takes place, incubation, originality and comparison take time, and top-down control and sensory gating might have to be more engaged (70, 73).

Although our results appear to contradict the often-cited positive association between executive functions and creativity (43, 44, 50), they may add to this line of research by showing that sensory and sensorimotor gating are differently related to creativity in comparison to executive functions. Speculatively, alternative protective mechanisms, such as increased working memory, well-developed executive functions or increased intelligence, in individuals with reduced sensory gating may allow them to benefit from their reduced filtering capacity during creative tasks. For instance, by allowing more stimuli to pass through the filter at an early stage in the attentional process which can be sufficiently processed thanks to well-developed executive functions and other protective mechanisms at later stages. However, if an individual suffers from substantial sensory gating deficits and has insufficient protective mechanisms to compensate for these deficits, then the outcome might still perhaps be increased creativity, but likely also accompanied by detrimental psychopathology (74, 75).

We found no association between attention or ADHD diagnosis, assessed by a parent questionnaire, and sensory or sensorimotor gating. Perhaps attentional difficulties do not originate from a general gating deficit but rather from a specific issue with controlled attention (76, 77). For instance, a sample of 10–12-year-olds with ADHD did not show any differences in PPI during a passive listening task but when participants had to actively ignore the stimuli, an attenuated PPI response was observed (78). Furthermore, adults with ADHD had a lower PPI response compared to healthy controls when task instructions were to attend to the stimuli in the paradigm, but no group differences were found during the passive listening condition (77). It is recommended that future studies compare both active and passive paradigms to detect possible differences in both creativity and attention. Indeed, it has been suggested that behaviourally observed attentional difficulties, as assessed in the current study, are more related to top-down attentional control deficiencies (79). Furthermore, while our attentional subscale of the behavioral questionnaire did not show a relation to sensory- and sensorimotor gating, there are indications that performance tests of attention do relate to P50 gating (25). Therefore, a more thorough investigation of different attentional measures and their relation to sensory- and sensorimotor gating is warranted. In addition, the hypothesis that creative individuals can flexibly alter their inhibitory and attentional processes based on task demands also fits well with this idea (2, 80).

By investigating different psychophysiological measures, our study further refined scientific knowledge about the often cited distractibility of creative individuals (9, 81). Results may help children that are easily distracted by motivating them in aspects of creativity and self-efficacy (82). However, the current study is not without its limitations. For instance, although we measured creativity in different ways, we did not include a specific convergent thinking task. Moreover, we did not collect data on parental mental history of the participating children. As a result, we cannot be sure that all parents were completely free of a psychiatric disorder, which may have influenced our data given that there are reports showing that offspring of patients with schizophrenia show less P50 suppression (83).

The sample size in the PPI analyses was rather small and the children that were unable to complete the PPI paradigm due to the stimulus intensity may all have had attenuated sensory gating. Therefore, we might have lost data from an important subgroup.

In conclusion, this study shows evidence that although sensory- and sensorimotor gating and attentional difficulties are unrelated, creativity and quantitative measures of divergent thinking such as fluency and flexibility, are at least indirectly related to decreased sensory, but not sensorimotor gating. In addition, lower sensorimotor gating seems to benefit tasks related to general creativity such as measured by our creative drawing task. Further research is required to examine if this relation is generalizable to other age groups, creativity measures, and measures of sensory gating.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the Faculty Ethics Review Board (FETC18-081) of the Faculty of Social and Behavioural Sciences at Utrecht University and the Medical Ethical Committee of the Utrecht Medical Centre (NWMO18-849). Written informed consent to participate in this study was provided by the participants' legal guardian/next of kin.

EK, BO, JV, and MS conceptualized the research. MS collected the data and wrote the original draft and edited the paper. MS and BO processed and analyzed the data. EK, JV, and BO critically reviewed the paper. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.