N=48 |
Mean |
SD |
Minimum |
Maximum |
Age |
36.19 |
9.9 |
23 |
57 |
Slant of the forehead degrees (SFD) |
17.73 |
5.49 |
10 |
34 |
UPPS-P Total (20-80) |
41.83 |
10.38 |
24 |
69 |
UPPS-P Negative urgency (4-16) |
9.79 |
2.81 |
5 |
16 |
UPPS-P Positive urgency (4-16) |
9.39 |
2.78 |
4 |
16 |
UPPS-P Sensation seeking (4-16) |
9 |
2.94 |
4 |
16 |
UPPS-P Lack of premeditation (4-16) |
7.22 |
2.41 |
4 |
15 |
UPPS-P Lack of perseverance (4-16) |
6.41 |
2.43 |
4 |
16 |
BIS11 Total (0-120) |
44.35 |
15.62 |
21 |
91 |
BIS11 Attention impulsiveness (0-32) |
13.77 |
4.55 |
6 |
27 |
BIS11 Motor impulsiveness (0-40) |
14.75 |
6.5 |
3 |
32 |
BIS11 Non-planning impulsiveness (0-48) |
15.83 |
7.04 |
1 |
34 |
SSS-V Total (0-40) |
20.22 |
7.05 |
5 |
32 |
SSS-V Thrill and adventure seeking (0-10) |
5.45 |
3.08 |
0 |
10 |
SSS-V Excitation seeking (0-10) |
6.35 |
2.12 |
2 |
10 |
SSS-V Disinhibition (0-10) |
4.25 |
2.2 |
0 |
9 |
SSS-V Boredom susceptibility (0-10) |
4.16 |
2.01 |
1 |
8 |
Table 2. Statistically significant negative correlations between cortical thickness and impulsiveness measures
Rostral anterior cingulate |
Isthmus cingulate |
Pericalcarine |
Inferior temporal |
Temporal pole |
||
Right |
||||||
UPPS-P |
-0.310 |
|||||
Lack of premeditation |
0.036 |
|||||
Left |
||||||
SSS-V |
-0.369 |
|||||
Excitation seeking |
0.012* |
|||||
Right |
Left |
Left |
Right |
|||
SSS-V |
-0.321 |
-0.338 |
-0.400 |
-0.411 |
||
Boredom susceptibility |
0.030* |
0.022* |
0.006* |
0.005* |
||
In each cell: hemisphere, Pearson correlation (adjusted by academic level and age), uncorrected p value *Significant after FDR correction. |
Table 3. Statistically significant positive correlations between cortical thickness and impulsiveness measures
Caudal anterior cingulate |
Caudal middle frontal |
Precentral |
Superior frontal |
Transverse temporal |
||
Right |
||||||
0.041 |
||||||
UPPS-P Total |
0.004* |
|||||
Right |
||||||
UPPS-P |
0.308 |
|||||
Positive urgency |
0.037 |
|||||
Right |
Left |
|||||
UPPS-P |
0.499 |
0.371 |
||||
Sensation seeking |
<0.0005* |
0.011* |
||||
Right |
Left |
|||||
UPPS-P |
0.380 |
0.292 |
||||
Lack of premeditation |
0.009* |
0.049* |
||||
Right |
||||||
UPPS-P |
0.319 |
|||||
Lack of perseverance |
0.031* |
|||||
Right |
Left |
|||||
BIS11 Total |
0.327 |
0.345 |
||||
0.026* |
0.019* |
|||||
BIS11 Attention impulsiveness |
Left |
Right |
Left |
|||
0.361 |
0.302 |
0.402 |
||||
0.017* |
0.041* |
0.006* |
||||
BIS11 Motor impulsiveness |
Left |
|||||
0.298 |
||||||
0.044* |
||||||
BIS11 Non-planning impulsiveness |
Right |
|||||
0.357 |
||||||
0.015* |
||||||
Right |
||||||
SSS-V Total |
0.300 |
|||||
0.043* |
In each cell: hemisphere, Pearson correlation (adjusted by academic level and age), uncorrected p value
*Significant after FDR correction.
Table 4. Statistically significant positive correlations between impulsiveness measures and slant of the forehead degrees
Slant of the forehead degrees |
|
UPPS-P Total |
0.534 |
<.0005* |
|
UPPS-P Positive urgency |
0.407 |
.005* |
|
UPPS-P Sensation seeking |
0.607 |
<.0005* |
|
UPPS-P Lack of premeditation |
0.522 |
<.0005* |
|
UPPS-P Lack of perseverance |
0.336 |
.023* |
|
BIS11 Total |
0.528 |
<.0005* |
|
BIS11 Attention impulsiveness |
0.556 |
<.0005* |
|
BIS11 Motor impulsiveness |
0.453 |
.002* |
|
BIS11 Non-planning impulsiveness |
0.392 |
.007* |
|
SSS-V Total |
0.585 |
<.0005* |
|
SSS-V Thrill and adventure seeking |
0.395 |
.007* |
|
SSS-V Excitation seeking |
0.425 |
.003* |
|
SSS-V Disinhibition |
0.502 |
<.0005* |
|
SSS-V Boredom susceptibility |
0.408 |
.005* |
In each cell: Pearson correlation (adjusted by academic level and age), uncorrected p value. *Significant after FDR correction.
Discussion
In this exploratory study we have found some significant correlations between the self-reported impulsiveness and cortical thickness in the prefrontal and temporal regions in healthy subjects. These findings are consistent with growing evidence of the influence of frontotemporal variations on impulsiveness. Furthermore, it is the first study which finds a positive correlation between the slant of forehead degree and the cortical thickness in prefrontal regions.
We also sought to obtain a higher self-reported representativeness of impulsiveness, which accounts for the 15 analyzed scores. In the exploration of the CT and its association with the UPPS-P model, we have found significant correlations in four scores. With respect to the negative ones, only the factor lack of premeditation has correlated with the right pericalcarine cortex. There exists scant evidence of the effect of pericalcarine cortex on impulsiveness, although some negative correlations have been found between the CT and the local gyrification index (LGI) in sensation seeking and attention impulsiveness (BIS) respectively (Holmes et al., 2016; Hirjak, et al., 2016). Despite the fact that the UPPS-P structural correlations are hardly known, this finding backs up former studies on significant morphological variations in the right pericalcarine cortex in terms of the presence of impulsive traits. However, we must point out that lack of premeditation has not been able to stand a statistical significance correction (FDR, p < 0.05).
In the UPPS-P questionnaire the positive correlations found must be highlighted. In particular the total scores and factors such as positive urgency, sensation seeking, lack of premeditation and lack of perseverance have correlated with the CT in the right caudal anterior cingulate cortex and, except positive urgency, all the above-mentioned factors have stood an FDR correction. These findings are in agreement with previous studies which, by using VBM, also found positive correlations between impulsiveness factors and GMV in right superior and middle frontal cortex, medial prefrontal cortex and posterior and anterior cingulate regions (Gardini et al., 2009; Cho et al., 2013). In the standard FreeSurfer atlas (Desikan et al., 2006), the caudal anterior cingulate cortex is part of the anterior cingulate cortex, whose region establishes significant associations between impulsive traits and morphological variations (Gardini et al., 2009; Matsuo et al., 2009; Thomann et al., 2015). Furthermore, the cingulate cortex has been associated with control of impulses, novelty seeking, persistence and impulsive behaviour (Bechara, 2005; Gardini et al., 2009). This finding may suggest that an increase in the CT of the right caudal anterior cingulate cortex exerts an influence on impulsiveness assessed with the UPPS-P model and, consequently, one might think of a consistent neuro-anatomical correlate found for this model.
On the other hand, the sensation seeking factor has also positively correlated with the left caudal middle frontal cortex. This region seems to be involved with cognitive control (Goghari and MacDonald, 2008) and inhibition of impulsive decisions (Essex et al., 2012). From this perspective it’s surprising that the left caudal middle frontal cortex has solely correlated with the sensation seeking factor out of the 15 scores analyzed. This seems to suggest a modest influence of the CT of the middle frontal cortex on the impulsive traits depicted in this study. Contrary to this finding, however, a negative association (Holmes et al., 2016) has previously been observed, which leads us to be very cautious about drawing conclusions. Furthermore, although the UPPS-P model is made up of our very different traits (Sharma et al. 2013) our exploration shows consistent evidence of a common neuroanatomical structure (right caudal anterior cingulate cortex) in five out of six scores of the model analyzed. Unlike some previous studies (Boes et al., 2009; Matsuo et al., 2009; Schilling et al., 2012; Tu et al., 2017) We did not find any negative associations between the CT and BIS. Our results show positive correlations (after FDR correction for all the scores) in influencing areas in the inhibitory control of impulsive conduct (superior frontal cortex and caudal anterior cingulate cortex). Which is consistent with earlier studies where the same association was found in prefrontal (Gardini et al., 2009; Cho et al., 2013; Du et al., 2016) and temporal (Schilling et al., 2012) areas. However, the heterogeneity of results of previous studies makes it difficult to draw some conclusions about the relationship between the variability in CT of prefrontal areas and BIS. Despite that our results in BIS seem to back up the evidence, independent of the CT, of the critical role of prefrontal and temporal structures. The correlation between the BIS total score with right caudal anterior cingulate cortex and left superior frontal cortex contrasts with the negative association found in left superior frontal cortex (Tu et al., 2017), which suggests, along with our findings, that variations in the left superior frontal cortex influence impulsiveness assessed with BIS total score. Another score, attention impulsiveness, not only correlates with the left superior frontal cortex, but also with the bilateral precentral cortex, a region which seems to be implicated in inhibitory control (Ma et al., 2012). This observation concerning the precentral cortex is consistent with previous studies, where positive associations with the impulsiveness in an adolescent sample were found by using VBM (Schilling et al., 2013b). The same association was found in the LGI in precentral and postcentral regions (Hirjak et al., 2016). Another factor that has correlated with the left superior frontal cortex has been motor impulsiveness. This finding is contrary to previous observations (Matsuo et al., 2009; Schilling et al., 2012). Even though our sample is comparable to previous studies, the factorial structure of the BIS-11 has been troublesome and the results derived from this self-report must be cautiously interpreted (Reid et al., 2013). Our findings in BIS show that variations in CT, in the left superior frontal cortex, can become an influencing structural correlation. Furthermore, the only scores that has not correlated with superior frontal cortex has been non-planning impulsiveness, an observation that is consistent with a previous study (Schilling et al. 2012). However, this factor has indeed correlated with the right caudal anterior cingulate cortex, where positive correlations have been found by using VBM (Cho et al., 2013; Gardini et al., 2009) as well as some variations in the LGI of frontal areas (Hirjak et al., 2016). This seems to indicate that regions of the cingulate cortex also exert their influence on non-planning impulsiveness.
Our latest self-report analyzed (SSS-V) showed four negative and one positive correlations, all of them in different brain regions (corrected results), which confirmed the higher number of negative correlations found in the three self-reports analyzed. With respect to the negative correlations, we have found a correlation between the ES and the CT in the left rostral anterior cingulate cortex. This finding can be expected given the influence of the cingulate cortex on impulsiveness traits (Gardini et al., 2009; Matsuo et al., 2009). What we found in the BS factor is more unexpected because of its correlation with four brain regions (right isthmus cingulate, right temporal pole, left temporal pole and left inferior temporal). This factor showed no correlations with the other three factors that make up SSS-V (Zuckerman et al., 1978). Together with our finding, this suggests that BS may be an independent factor where reductions in the CT of temporal and posterior regions of the cingulate cortex could be implicated in this trait. Therefore findings in right temporal pole, left temporal pole and left inferior temporal cortex support former studies on the importance of temporal regions in the manifestation of impulsive traits (Gardini et al., 2009; Hanford et al., 2016; Hirjak et al., 2016; Schilling et al., 2012; Schilling et al., 2013b), including general impulsiveness (Lyoo et al., 2006). They also support the evidence that impulsiveness is not exclusively under the control of the prefrontal cortex (Braquehais et al., 2010).
On the other hand, TAS is regarded as a non-impulsive way of seeking sensations (Zuckerman, 1983). Oddly enough, TAS did not correlate with any brain structures in our study. This finding can support Zuckerman’s TAS and back up the idea of the uses of the factors ES and BS as an equivalent measurement for impulsiveness. Although the sensation seeking trait and impulsiveness have distinct developmental trajectories (Steinberg et al., 2008), they can share a common neuroanatomical structure as well as underlie the same neurobiology (Holmes et al., 2016). Considering the influence exerted by impulsiveness on the sensation seeking trait (Eysenck and Eysenck, 1985), it would back up the use of SSS-V as an equivalent measurement to impulsiveness.
On the other hand, SSS-V total score has only correlated with right caudal anterior cingulate cortex (corrected result), which supports the evidence shown in this study concerning the influence of this region on the impulsive traits. In this sense, it is worth highlighting that right caudal anterior cingulate cortex has correlated with eight scores, including the total score of the three self-reports analyzed.
With respect to our secondary objective, this is the first study that explores the SFD with the CT of the entire cortex. Our finding of the positive correlations between SFD and the CT in prefrontal regions (Figure 2) with self-reported impulsivity supports the growing body of scientific evidence of the influence of these regions on the self-reported impulsiveness. Based on our data it seems that SFD can influence the CT in frontal but not posterior regions of the brain. However, the complexity in discussing these findings is obvious and more studies need to be carried out in order to draw consistent conclusions. It appears that the frontal lobes influence the shape of the forehead and a higher development in of the frontal protuberance (bulky superciliaries) results in a higher slant (Balueva and Lebedinskaya, 1991). Likewise, subjects with protruding superciliar structure seem to report structure seem to report a higher obstinacy in their behaviour (Han and Park, 2014). This observation is consistent with Pujol, et al. (2011), where it was found that more compulsive subjects, therefore, possibly more impulsive (Voltas-Moreso et al., 2013) presented with a lengthening pattern in the space of the cerebral-spinal fluid of the frontal operculum which correlated positively with the frontal protuberance (superciliary arches). Together with our finding, it is necessary to point out that previous studies suggest that the structure of the face can facilitate information about the brain (Sisodiya et al., 2008) or that the face, the craniofacial skeleton and the central nervous system have an interconnected development (Kjaer, 1995).
Some limitations to our study must be duly considered. First, we did not control the consumption of tobacco or other substances A factor that is strongly associated with externalization or disinhibitory disorders (alcohol dependence, drug taking or behaviour disorders) is negative urgency of the model UPPS-P (Settles et al., 2012), where no correlation was found.
Second, the size of the sample was modest, which limits the generalization of our results. However, the number of participants is similar to comparable former previous studies (Kumari et al., 2009; Schilling et al., 2012).
Third, our study has focused on subjective impulsiveness measurements and, despite being described as an efficient method (Mathias et al., 2008), it would be convenient to replicate or refute our findings with objective measurements since there exists the evidence of no correlation between objective measurements and GMV in frontal areas (Tschernegg et al., 2015). That is why we must be cautious and limit our findings to the instruments used rather than to impulsiveness broadly speaking.
Finally, despite the existence of individual differences in the profile view of the slant of the forehead (Adams et al., 2013; Oh et al., 2016; Guerrero et al., 2016; Guerrero et al., 2018a,) an aspect that can trigger some controversy is the anthropometric measurement SFD. However, a recent study found a high level of interobserver agreement in the visual assessment of the level of the forehead slant, whose measurement obtained a high correlation with the anthropometric SFD measurement (Guerrero et al., 2016; Guerrero et al., 2018a). This backs up the validity of the anthropometric SFD measurement used in this study. Furthermore, in our SFD measurement the NHP has been taken into account, usually used in profile photographs in order to control the placement of the reference points in teleradiography (Lundstrom, et al., 1995).
In conclusion, our exploration supports the growing evidence of the importance of the CT variations in frontal and temporal areas in the assessment of self-reported impulsiveness among healthy subjects. If we consider that the morphology of craniofacial structures and that of the brain is interwoven in a complex fashion (DeMyer, 1975), then we can suggest a relationship between the slant of the forehead and the CT variations in frontal regions. However, this preliminary finding must be taken cautiously and we must and observe the results of future investigations. We suggest that a new line of research could be opened about the importance of SFD in the manifestation of the impulsive behavior in healthy subjects, as well as about the relationship between SFD and structural and functional aspects of the underlying brain tissue. Thus, this study examined the cortical thickness correlates of auto-report impulsiveness, demonstrating that prefrontal and temporal regions are crucial for impulsiveness in healthy adults. Likewise, the slant of the forehead is associated with the thickness of crucial cortical regions for impulsiveness traits.
The authors declare no competing financial interests.
Abbreviations: BIS-11: Barratt Impulsiveness Scale; BS: Boredom Susceptibility; CT: Cortical Thickness; DIS: Disinhibition; ES: Experience Seeking; G: Glabella; GMV: Gray Matter Volume; NHP: Natural Head Position; TAS: Thrill And Adventure Seeking; TR: Triquion; SBM: Surface-Based Morphometry; UPPS-P: Short Scale of Impulsive Behaviour; SFD: Slant Of The Forehead Degree; SSS-V: Zuckerman Sensation Seeking Scale V; TV: True Vertical; VBM: Voxel Based Morphometry
Acknowledgements
We are really grateful to Javier González Zabaleta, CEO in Medimsight, for his professionalism. Also, our heartfelt thanks to the developer LAIMBIO, from the URJC. To be grateful for the contribution of Dr. J B. Navarro-Pastor in the analysis of data. And also, to be thankful for the support of Dr. Julián Gabarre Mir in part of the sample recruitment, and magnetics resonances acquisition. As well as, to all the volunteers who participated in this study.
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