Imagination task

One of four experimenters (two females and two males) approached 376 subjects (188 females and 188 males) aged approximately 20–30 years in various locations on the University campus, malls and other places where they could sit comfortably. Since neither invasive nor risky procedures were involved and since the data were analyzed anonymously, participants were required to give only oral consent. The study was carried out in accordance with the principles of the Declaration of Helsinki and following the approval of the local ethical committee (Comitato Etico d'Ateneo, Università “G. d'Annunzio” – Chieti).

The experimenter, standing in front of the participant, made sure that the subject placed her/his hands palm-down on the knees or on a table, and that she/he did not cross her/his legs, arms or even fingers. Then the experimenter invited the participant to close her/his eyes and to imagine a female or male person seen from behind, without giving any further clue on the identity of the person to be imagined. Once the participant stated to ‘see’ the person, the experimenter asked her/him to imagine that the person was performing an action. Thereafter, when the participant stated to ‘see’ the person's movement clearly, the experimenter asked her/him to open her/his eyes and to indicate the hand used by the person by showing her/his own right or left hand. Only one trial was administered to each participant. The trial took around 3–4 minutes to be accomplished. In order to assess the participant's hand preference, she/he was administered the Italian version of the Edinburgh Handedness Inventory [53], which measures laterality as a continuous variable ranging from -1 to +1 (from complete left-handedness to complete right-handedness).

Three groups of participants were asked to imagine a person performing one of these three actions: using scissors (120 subjects), using a toothbrush (112 subjects) or using a spoon (144 subjects). Each group was composed of an identical number of:

• females imagining a female person;
• females imagining a male person;
• males imagining a female person;
• males imagining a male person.

Only subjects who were able to ‘see’ the person and the person's movement and to clearly indicate a definite (right or left) hand for the imagined action were included in the study. Of all subjects who succeeded in performing the task, none spontaneously reported having imagined her/himself as the person performing the movement, and only few subjects reported having imagined a familiar person.

Self-reported empathy

After completing the handedness questionnaire, participants were administered the Italian versions of the Interpersonal Reactivity Index (IRI; [54]) and the Balanced Emotional Empathy Scale (BEES; [55]).

The IRI [51] is a 28-item questionnaire consisting of four discrete, seven-item subscales assessing different dimensions of empathy: Perspective Taking (PT), Fantasy (FS), Empathic Concern (EC), and Personal Distress (PD).

The BEES [52] is a 30-item questionnaire that assesses the tendency to share the emotional experiences of others, and represents a measure of emotional empathy.

More detailed descriptions of both questionnaires are available as Supporting Information (Text S1).

Data analysis

According to the laterality score obtained in the Italian version of the Edinburgh Handedness Inventory [53], the 376 participants were divided into two categories: right-handers (345 subjects with a positive laterality score [range: 0.04/1.00; M = 0.67±0.013 SEM]) or left-handers (30 subjects with a negative laterality score [range: −1.00/−0.03; M = −0.55±0.052 SEM]). One female participant with a laterality score equal to 0 was excluded from data analyses.

As in our previous study [31], the proportion of matches vs mismatches between participants' dominant hand and the hand used by the imagined agent did not differ across actions (χ² = 1.623, d.f. = 2, p = 0.444; Table 1), so we did not consider the variable Action in the following analyses.

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Table 1. Proportion of matches vs mismatches between participants' dominant hand and the hand used by the imagined agent for the different actions.

https://doi.org/10.1371/journal.pone.0014595.t001

Imagination task

Compared to a chance distribution (50%), right-handers imagined a higher proportion of right- than left-handed actions (313 vs 32 [90.7%]; χ² = 228.872, d.f. = 1, p<0.001), while left-handers imagined a larger proportion of left- than right-handed actions, although this difference was not significant (17 vs 13 [56.7%]; χ² = 0.533, d.f. = 1, p = 0.465). Moreover, right-handers showed a larger proportion of matches vs mismatches between their dominant hand and the hand used by the imagined agent compared to left-handers (χ² = 27.177 [Continuity Correction Applied, from now on: CCA], d.f. = 1, p<0.001).

The proportion of matches vs mismatches did not differ according to either the participants' sex (females: 162 vs 25 [86.6%]; males: 168 vs 20 [89.4%]; χ² = 0.429 [CCA], d.f. = 1, p = 0.513) or the correspondence between the participants' sex and the imagined agent's sex (same sex: 167 vs 21 [88.8%]; opposite sex: 163 vs 24 [87.2%]; χ² = 0.113 [CCA], d.f. = 1, p = 0.736).

When participants were divided according to their lateral preference for the specific action imagined (using scissors, using a toothbrush, or using a spoon) as declared in the handedness questionnaire rather than total laterality score obtained by considering all items, results were almost identical. However, this choice would have entailed the loss of 30 participants who indicated no lateral preference for the particular action imagined, so we decided to report only the results of analyses employing total laterality score as the criterion for defining handedness.

IRI susbscales

The only significant effect was that of Sex (F_4,317 = 3.281; p<0.05). Post hoc univariate analyses showed that females (n = 163) scored significantly higher than males (n = 162) in the EC subscale (M_f = 28.63 vs M_m = 25.77; F_1,320 = 10.472; p<0.005), and a statistical trend in the same direction was observed in the PD subscale (M_f = 19.32 vs M_m = 17.44; F_1,320 = 3.108; p = 0.079), while there were no differences in the PT subscale (M_f = 25.89 vs M_m = 24.12; F_1,320 = 1.165; p = 0.281) and in the FS subscale (M_f = 24.49 vs M_m = 22.45; F_1,320 = 2.368; p = 0.125; Figure 1).

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Figure 1. Female and male participants' scores on the IRI subscales (PT: Perspective Taking; FS: Fantasy; EC: Empathic Concern; PD: Personal Distress).

https://doi.org/10.1371/journal.pone.0014595.g001

BEES

Statistical analyses showed significant main effects of both Sex (F_1,347  =  13.798; p<0.001) and Lateral Correspondence (F_1,347 = 4.023; p<0.05): females scored higher (n = 178; M = 37.56) than males (n = 174; M = 18.93), and participants who imagined the action being performed with their dominant hand scored higher (n = 309; M = 29.17) than those who imagined the action being performed with their non-dominant hand (n = 43; M = 22.44).

A significant interaction between Sex and Lateral Correspondence (F_1,347 = 10.467; p<0.005) showed that the previous results were due to females who imagined the action being performed with their dominant hand scoring significantly higher (n = 154; M = 39.79) than all the other groups (females, non-dominant: n = 24, M = 23.25; males, dominant: n = 155, M = 18.62; males, non-dominant: n = 19, M = 21.42; all ps<0.001; p values adjusted with the Tukey-Kramer method), while there were no differences between these latter groups (Figure 2).

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Figure 2. BEES scores as a function of Sex and Lateral Correspondence (D: dominant hand; ND: non-dominant hand).

https://doi.org/10.1371/journal.pone.0014595.g002

Imagination task

With regard to participants' responses in the imagination task, the present results confirm those of our previous study [31]: 1) both right-handers and left-handers preferentially imagined actions performed with their dominant rather than non-dominant hand (although this difference was significant only for right-handers, possibly because the number of left-handed participants was not sufficient to detect a rather moderate difference); 2) compared to left-handers, right-handers reported a larger proportion of matches between their dominant hand and the hand used by the imagined agent. As already proposed [31], the lower proportion of matches vs mismatches in left-handers may be attributed to both their greater visual familiarity with actions performed with their non-dominant hand (inducing an incongruence between the visual experience of others' actions and one's own experience of self-made actions) and their lower average absolute degree of lateralization, in line with previous research showing handedness-related differences with regard to motor representations in both behavioral and functional measures[56]–[58].

Self-reported empathy

Compared to males, females exhibited higher empathy scores, and the difference was particularly significant for the emotional component of empathy, as apparent in participants' responses to the IRI EC subscale and the BEES. This is consistent with past research employing self-report data [59]–[61].

Our results provide good (albeit not complete) support for the hypothesis that participants imagining actions performed with their dominant hand would exhibit higher empathy compared to those imagining actions performed with their non-dominant hand. In fact, the effect of lateral correspondence was due exclusively to women, because female participants who imagined actions performed with their dominant hand scored higher on the BEES than all other groups, which did not differ between each other.

If one assumes that the lateral congruence between one's own and an imagined agent's handedness can be considered as indicative of a greater involvement of motor areas compared to the lateral incongruence, our results are consistent with previous research suggesting a link between empathic tendencies and the activation of motor-related areas [14]–[19], [28]–[30]. In particular, it is important to note that much research indicates a stronger activation of motor representations during emotional and empathic processes in women than in men. For example, females exhibit more pronounced and more congruent facial electromyographic reactions to observed facial expressions than males [62]–[64]. Compared to men, women show enhanced MNS activation during emotional perspective taking, which may be related to gender differences in the tendency to exhibit facial mimicry [65]. Moreover, during the simple observation of leg and hand movements as well as during the observation of body parts in both painful and non-painful situations, activity in the MNS (as indicated by mu rhythm suppression) is stronger in females than in males [66]–[69]. Interestingly, there is some evidence that such activity is positively correlated with self-reports of empathy in females but not in males (i.e., painful condition in [69]; for congruent findings, see [70]). Overall, these studies strongly suggest that females activate motor-related areas more than males during emotional and empathic processing, consistent with neuroimaging research indicating that females and males rely on different neural strategies for these tasks (e.g., [71]–[75]).

Furthermore, females and males report using respectively egocentric strategies and object-based strategies when performing visuospatial perspective-taking tasks, and these preferences appear to be associated with the recruitment of specific brain regions [26], [76]. Congruent differences are also found for egocentric mental rotation of hands, females relying more on imitation or perceptual comparisons (as suggested by stronger activity in the left ventral premotor cortex), and males relying more on early visual or semantic processing (as suggested by stronger activity in the lingual gyrus) [77]. Moreover, females seem to engage more emotion and self-related processes and males more cognitive processes during tasks involving both affective and cognitive empathy, even in the absence of significant gender differences in behavioral performance [78]. Finally, an intriguing instance of more strongly embodied representations in females than in males can be observed in giving route directions, a task in which women are more concrete and personal, using landmarks and left–right terms, whereas men are more abstract and Euclidean, using cardinal directions and metric distances [79] (see also [80], for an interesting correlation between anxiety during environmental navigation and way-finding strategies). In sum, it is plausible that the gender-specific result found in our study may be a consequence of the stronger involvement, in more empathic females, of motor- and self-related processes, which could result in more body-specific (see [81]) and ‘concrete’ imagery.

Noteworthy, a significant link between the hand used by the imagined agent and self-reports of empathy was found when examining the BEES [52] scores, but not when examining any IRI [51] subscale scores. This result makes sense if one considers that different dimensions of empathy are measured by these instruments. In fact, as regards the IRI [51], while the PT and FS subscales assess cognitive empathy, the EC subscale assesses the tendency to sympathize with and be concerned about others, and the PD subscale assesses the tendency to feel negative emotions in response to others' distress. On the other hand, the BEES [52] assesses the tendency to vicariously experience both positive and negative emotions of others, and thus could provide a more specific measure of affective sharing. Therefore, compared to any IRI subscale, the BEES might prove to be a more sensitive marker of the tendency to engage motor representations, because affective empathy seems to activate motor-related areas more intensely than cognitive empathy [22].

Since, in line with some studies reporting a left hemisphere dominance for empathic abilities in right-handers [26], [82], we observed a positive correlation between female participants' laterality scores and BEES scores (see Supporting Information, Text S2 and Figure S1) and, in line with our previous study [31], absolute laterality score was positively associated with the likelihood to imagine an action performed with one's own dominant rather than non-dominant hand (see Supporting Information, Text S3), the positive association between lateral correspondence and the BEES scores observed in our female participants might be attributed to the covariance of both these variables with laterality scores, the great majority of our participants being right-handed. However, this possibility can be ruled out because a significant interaction between Sex and Lateral Correspondence was also found when the analysis (employing Laterality Score as a covariate) was carried out for right-handers only (see Supporting Information, Text S3 and Figure S2).

A possible concern regarding the procedure used to investigate our hypotheses could consist in the fact that we asked our subjects to ‘see’ an imagined person performing an action, which might seemingly engage visual rather than motor imagery. Since visual imagery is usually associated with brain areas – mainly not motor – different from those associated with motor imagery (e.g., [83], [84]), one could wonder why a visual imagery task should have tapped motor representations (and thus the allegedly motor neural basis of empathic abilities). However, we point out that, as well as during others' action perception (see [42] for a review), the activation of motor representations is found during the imagination of not only one's own (e.g., [39], [41]) but also of others' movements (e.g., [40]). In particular, as regards the link between empathic abilities and the recruitment of motor representations, a positive correlation between self-reports of empathy and neural activity in regions of the MNS has been reported for different tasks, including tasks which might involve mainly visual representations (i.e., the observation of pleasant and unpleasant emotions [17]) or even the mere imagination of others' behavior (i.e., the anticipation of others' emotional responses [15]). So, it is plausible that empathic tendencies could affect performance in an imagination task which is deemed to involve one's own motor representations [40] (see also [31] for consistent behavioral results).

In conclusion, the present study corroborates our hypothesis that self-reported empathy is positively linked to the activation of motor representations while imagining another person performing an action. However, this relationship seems to be present only in female subjects, consistent with previous research indicating a stronger involvement of action representations during emotional and empathic processing in females than in males [62]–[65]. In other words, compared to male participants, female participants were likely to use more self- and motor-related representations during the imagination task, which is consistent with neuroimaging findings on gender-specific neural activity during both visuospatial and emotional perspective taking [65], [76], [78].

Finally, our results underline the possibility of employing behavioral research as a test-bed for theories deriving from functional studies. Conversely, a possible extension of this study could consist in employing neuroimaging techniques such as fMRI and TMS in order to test the proposed correlation between self-reported empathy and body-specific motor representations [81] during others' action imagination.