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The role of embodied simulation in mental transformation of whole-body images: Evidence from Parkinson’s disease
Human Movement Science 33 (2014) 343–353
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The role of embodied simulation in mental transformation of whole-body images: Evidence from Parkinson’s disease Massimiliano Conson a,⇑, Luigi Trojano a,b, Carmine Vitale c,d, Elisabetta Mazzarella e, Roberto Allocca f, Paolo Barone c,g, Dario Grossi a, Gabriella Santangelo a,c,⇑ a
Neuropsychology Laboratory, Department of Psychology, Second University of Naples, Viale Ellittico 31, 81100 Caserta, Italy Salvatore Maugeri Foundation, IRCCS Institute of Telese Terme (BN), Italy IDC ‘‘Hermitage-Capodimonte’’, Naples, Italy d University of Naples Parthenope, Naples, Italy e Department of Neuromotor Physiology, Scientific Institute Foundation Santa Lucia, Via Ardeatina 306, 00179 Rome, Italy f Department of Neurological Sciences, University Federico II, Naples, Italy g Neurodegenerative Diseases Center, University of Salerno, Salerno, Italy b c
a r t i c l e
i n f o
Article history: Available online 26 November 2013 PsycINFO classification: 2520 Neuropsychology & Neurology Keywords: Embodied cognition Action simulation Mental transformation Parkinson’s disease Mental rotation Motor imagery
a b s t r a c t It has been repeatedly demonstrated that mentally performing an action and mentally transforming body-parts entail simulation of one’s own body movements, consistent with predictions of embodied cognition theories. However, the involvement of embodied simulation in mental transformation of whole-body images is still disputed. Here, we assessed own body transformation in Parkinson’s disease (PD) patients with symptoms most affecting the left or the right body side. PD patients were required to perform left– right judgments on front-facing or back-facing human figures, and a letter rotation task. Results demonstrated that PD patients were selectively impaired in judging the side of back-facing human figures corresponding to their own most affected side, but performed as well as healthy subjects on mental transformation of front-facing bodies and on letter rotation. These findings demonstrate a parallel impairment between motor and mental simulation mechanisms in PD patients, thus highlighting the specific contribution of embodied cognition to mental transformation of whole-body images. Ó 2014 Published by Elsevier B.V.
⇑ Corresponding authors at: Neuropsychology Laboratory, Department of Psychology, Second University of Naples, Viale Ellittico 31, 81100 Caserta, Italy. Tel.: +39 0823 275327. E-mail addresses: [email protected] (M. Conson), [email protected] (G. Santangelo). 0167-9457/$ - see front matter Ó 2014 Published by Elsevier B.V. http://dx.doi.org/10.1016/j.humov.2013.10.006
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1. Introduction Classical psychophysical studies showed that when healthy participants have to judge whether a hand image with a specific spatial orientation is left or right (i.e., the hand laterality task) they imagine their own hand moving to match the stimulus orientation for responding (Parsons, 1987a, 1994; Sekiyama, 1982). Moreover, making hand laterality judgments and executing a hand movement follow the same temporal profile and the same hand-specific joint-constraints (Conson, Mazzarella, & Trojano, 2011; de Lange, Helmich, & Toni, 2006; Parsons, 1987a, 1994; Sekiyama, 1982). Accordingly, specific impairments on the hand laterality task and spared mental transformation of object images have been reported in patients with severe motor disorders, such as locked-in syndrome (Conson, Pistoia, Sarà, Grossi, & Trojano, 2010; Conson et al., 2008), amyotrophic lateral sclerosis (Fiori et al., 2013a) or spinal cord injury (Fiori et al., 2013b). These observations consistently support the model of embodied cognition according to which cognitive processes are grounded in bodily states (Gallese & Sinigaglia, 2011). In this view, the same sensorimotor representations activated when performing an actual action are also involved in different ‘‘action-related phenomena’’ such as motor imagery (i.e., mental simulation of body-parts movements), action observation and imitation (Decety & Grèzes, 2006; Gallese & Sinigaglia, 2011; Jeannerod, 2001). No clear data are available instead on the role of embodied simulation in mental transformation of whole-body images. In a seminal neuroimaging study, Zacks, Rypma, Gabrieli, Tversky, and Glover (1999) presented participants with front-facing or back-facing schematic human figures with one outstretched arm; in order to judge which arm was outstretched (i.e., left–right judgment), participants imagined themselves in the position of the figure. This own body transformation led to increased cortical activity in the temporo-parietal junction, as well as in other areas including the frontal cortex. Subsequent neurofunctional studies employing the same paradigm (Arzy, Mohr, Michel, & Blanke, 2007; Arzy, Thut, Mohr, Michel, & Blanke, 2006; Blanke et al., 2005) confirmed the involvement of the temporo-parietal junction in whole-body processing and suggested that whole-body transformations imply some sort of ‘‘rotation of the self’’ (Arzy et al., 2006, 2007; Blanke et al., 2005). This evidence would suggest that, analogously to body-parts transformation, mental transformation of whole-body is grounded on embodied cognitive processes (Kessler & Thomson, 2010). However, other studies demonstrated that whole-body transformation can also be accomplished by resorting to an object-based, visuospatial transformation not related to one’s own body representation (Gardner, Brazier, Edmonds, & Gronholm, 2013; Kessler & Wang, 2012). For instance, Kessler and Wang (2012) reported that healthy individuals with low empathic abilities were more prone to rely on object rotation strategies to solve the own body transformation task. These findings would undermine the idea that whole-body transformation is dependent on actual sensorimotor information available in the agent’s brain. In synthesis, the role of embodied simulation in whole-body transformation is not supported consistently. Strong clues on this issue could be provided by a behavioral study on patients with a welldefined damage of the motor system, such as Parkinson’s disease (PD). Neuropsychological studies investigating mental transformation of body-parts in PD patients by means of the hand laterality task reported motor imagery asymmetries: patients mentally simulated movements more slowly with their most affected hand (Amick, Schendan, Ganis, & Cronin-Golomb, 2006; Dominey, Decety, Broussolle, Chazot, & Jeannerod, 1995). These results were confirmed by recent experiments in which PD patients performed the hand laterality task while keeping their arms in different postures (Helmich, de Lange, Bloem, & Toni, 2007; van Nuenen et al., 2012). Taken together, available evidence supported the strong relationships between motor disorders and mental transformation of body-parts in PD patients. However, no evidence is available about mental transformation of whole-body images in this clinical population. In the present study we required PD patients to perform own body transformation tasks requiring laterality judgments on a schematic human figure. If sensorimotor information is causatively involved in processing of whole-bodies, we can predict that PD patients would be impaired on own body transformation task, and that the side of motor impairment would affect behavioral performance, with opposite patterns in patients with left or right most affected side. More precisely, consistent with previous studies on mental transformation of body parts (Helmich et al., 2007; van Nuenen et al., 2012),
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we could expect that PD patients are specifically impaired in judging the body side corresponding to their own most affected side. Relevant here, we also assessed PD patients’ ability to perform mental rotation of letters that is thought not to involve one’s own body representation (Conson et al., 2008, 2010; Dalecki, Hoffmann, & Bock, 2012; Fiori et al., 2013a, 2013b; Kosslyn, Di Girolamo, Thompson, & Alpert, 1998). By these means we could ascertain whether any failure in own body transformation was associated with a generalized deficit in performing mental transformation tasks. 2. Material and methods 2.1. Participants We screened consecutive PD patients attending the Movement Disorders Unit of the University of Naples Federico II (Naples, Italy) from February to June 2012. Patients were enrolled in the study if they met the following inclusion criteria: diagnosis of idiopathic PD according to United Kingdom Parkinson’s Disease Society brain bank (Gibb & Lees, 1988); clinical and history evidence of asymmetric motor disturbances; lack of PD-associated dementia (PDD) as diagnosed according to an algorithm for clinical diagnosis of PDD recommended by the MDS Task Force (Emre et al., 2007); lack of major depression according to DSM IV criteria (American Psychiatric Association, APA, 1994). All PD patients underwent a neurological examination including the Unified Parkinson’s Disease Rating Scale motor subscale (UPDRS-III; Fahn, Elton, & Members of the UPDRS Development Committee, 1987) to evaluate severity of motor symptoms, and Hoehn & Yahr Scale (H&Y; Hoehn & Yahr, 1967) to assess PD stage. Age, level of formal education, age at onset, side of onset of PD, disease duration, and type and dosage of pharmacological treatment were recorded; Levodopa equivalent daily dose (LEDD) was calculated (Tomlinson et al., 2010). As a screening for general cognitive impairment we used an Italian version of the Mini Mental State Examination (MMSE), and excluded from the study PD patients with a total age- and educational-adjusted score <23.8, that is the standard cut-off for the normal range (Folstein, Folstein, & McHugh, 1975; Measso et al., 1993). Twenty-nine right-handed patients (10 females and 19 males) matched inclusion and exclusion criteria. Mean patients’ age was 67.6 ± 7.7 years (range 54–83 years) and mean educational level was 10.9 ± 4.9 (range 3–18 years). In the total sample, mean age at onset was 60.7 ± 8.5 (range 44–77 years) and mean disease duration was 7 ± 4.3 years (range 2–21 years), respectively. Mean UPDRS-III scores were 14.1 ± 4.9 (range 6–28). H&Y rating scale ranged from Stage I to Stage III. Mean total LEDD was 621.5 ± 295.6 mg (range 150–1300). Side of onset of motor symptoms and of most severe motor disturbances on repeated clinical assessment (most affected side) was the left in 14/29 patients (left-most affected PD: 48.3%) and the right in 15/29 (right-most affected PD: 51.7%) patients. No significant differences between the two groups were found on demographic and clinical features (Table 1). PD patients underwent the experimental tasks (see below) when they were in the ‘‘on’’ phase. Thirty right-handed healthy subjects (10 females and 20 males; mean age 49.7 years, SD 7.3, range 46–83 years; mean education 14.7, SD 2.5, range 11–18 years) took part in the experiment as healthy controls. Exclusion criteria were the following: (1) diagnosis of PD or any other neurologic or psychiatric disorder; (2) clinically evident dementia or major depression, both diagnosed by means of DSM IV criteria (APA, 1994); (3) general intellectual impairment, defined by MMSE score below the normal cut-off, as above. The study was conducted in accordance with the ethical standards of Helsinki Declaration and an informed consent was obtained from all participants after the nature of the study was fully explained to them. 2.2. Experimental tasks Participants underwent the classical own body transformation task (OBT; Arzy et al., 2006; Blanke et al., 2005; Parsons, 1987b; Zacks et al., 1999), requiring left–right judgments on a human image whose left or right hand was marked to appear as wearing a black glove. After imagining themselves to be in the figure’s body position and to have its visual perspective, participants had to judge whether
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Table 1 Mean (±SD) of demographic and clinical features of PD patients.
Age (yr) Education (yr) Sex (M/F) Age at PD onset (yr) PD duration (yr) UPDRS-III score in on-state H&Y score Total-LEDD (mg/d) Dopamine agonist LEDD (mg/d) Patients receiving levodopa monotherapy Patients receiving dopamine agonist monotherapy Patients receiving combination agonist and levodopa therapy
Left-most affected PD (n = 14)
Right-most affected PD (n = 15)
F/U test
P
62.9 ± 4.7 10.8 ± 5.8 8/6 61.8 ± 8.4 7.5 ± 5.1 12.9 ± 4.1 1.9 ± 0.6 626.8 ± 328.5 483.3 ± 360.5 5 3 6
66 ± 8.6 11 ± 4.8 11/4 59.7 ± 8.7 6.6 ± 3.5 15.4 ± 5.6 1.7 ± 0.6 616.7 ± 278 340 ± 218.1 2 2 11
1.347 .015 .840 .442 .310 1.767 93 .008 1.490
.256 .904 .359 .512 .582 .195 .621 .929 .235
Yr = years; PD = Parkinson’s disease; UPDRS-III = Unified Parkinson’s disease rating scale; H&Y = Hohen & Yahr; Total LEDD = Total L-Dopa equivalent daily dose.
the left or the right hand of the human figure was marked. Human images were displayed facing toward (front-facing-OBT) or away from the observers (back-facing-OBT). The back-facing orientation is compatible with the participants’ perspective, whereas in the front-facing orientation the observers have to imagine their own bodies into the position of the front-facing human figure to perform the left/right judgment. Following previous studies (Arzy et al., 2006; Blanke et al., 2005; Zacks et al., 1999), task instructions explicitly required participants to mentally simulate one’s own body movement. By these means, we could induce subjects to resort to one’s own body representation during task performance (see Hétu et al., 2013, for a discussion on explicit versus implicit motor imagery). Participants also completed a letter rotation task (LRT), requiring whether a capital letter was presented in canonical or mirror-reversed form (Conson et al., 2008). The three tasks (i.e. front-facingOBT, back-facing-OBT and LRT) were administered by means of a computerized procedure, and were arranged to be as similar as possible in presentation and response modalities, although specific instructions differed.
2.3. Stimuli and procedure Stimuli consisted of line drawings depicting front-facing or back-facing body images whose right or left hand was marked in black, or of letters in canonical or mirror-reversed form. All stimuli were presented in four spatial orientations: 0°, 90° clockwise (cw), 90° counterclockwise (ccw) and 180° (Fig. 1). Stimuli were large approximately 8 cm along the widest axis (about 7.6° of visual angle at a viewing distance of 60 cm from a 15’’ computer screen) and were presented at the centre of the monitor until response completion; each stimulus was preceded by a fixation point (1000 ms). Patients and healthy controls gave their responses by pressing one of two centrally located keys (B and H keys on QWERTY keyboard) with their index and middle fingers of the right (dominant) hand; the stimulus-response association for each task was counterbalanced across participants. The left hand was placed in a comfortable position, palm down next to the keyboard. Following classical studies (e.g., Sekiyama, 1982), both hands were covered with a black cloth in order to avoid that visual cues provided by one’s own hands could facilitate left–right judgments on body images (for instance see Ionta & Blanke, 2009 for recent data on the role of visual familiarity on mental transformation of body-parts). Participants were encouraged to respond as fast and correctly as possible; we recorded both Reaction Times (RTs, in milliseconds) and accuracy. Stimulus presentation and data collection were controlled by a PC using Cedrus SuperLab v.4. Each task (front-facing-OBT, back-facing-OBT and LRT) consisted of 48 trials: in both front-facingand back-facing-OBT, six trials were presented for each combination of hand laterality (left or right)
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Fig. 1. Instances of stimuli used in the three mental transformation tasks: front-facing-OBT (first row), back-facing-OBT (second row), and letter rotation task (LRT, third row), in the four spatial orientations: 0°, 90° clockwise (cw), 90° counterclockwise (ccw) and 180° (schematic human figures with their left hand marked in black, and letters in mirror-reversed form are not reported here).
and spatial orientation; in the LRT, six trials were presented for each combination of type of stimulus (canonical or mirror-reversed) and spatial orientation. Trials were randomized within each task, which was divided in two blocks, with a 3-min pause allowed between the two blocks. A training period preceded the experiment. Before starting each task, eight practice trials were given; if a wrong response was provided, feedback appeared on the monitor screen and the trial was repeated. Experimental session started only if the participants provided at least six consecutive correct responses. Testing was conducted in a quiet room and in a single session that lasted about 20 min; the order of the three tasks was counterbalanced across participants. 2.4. Statistical analysis First, Pearson’s correlations between accuracy and RTs were calculated for each mental rotation task in each group to assess whether participants’ performance showed any speed-accuracy tradeoff (Sanders, 1998). Then, overall mean RTs and accuracy were analyzed by means of separate twoway mixed Analysis of Variance (ANOVA), with task (front-facing-OBT, back-facing-OBT and LRT) as a within-subject factor and with group (healthy participants, left-most affected and right-most affected PD patients) as a between-subject factor.
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To ascertain the involvement of embodied processing in whole-body transformation, we tested whether the side of prevalent motor impairment in PD patients specifically affected performance on the corresponding side of the human figure in the OBT tasks. To this aim, a four-way mixed-design ANOVA was performed on correct RTs and accuracy, with task (front-facing-OBT or back-facing-OBT), side of marked hand (left or right) and spatial orientation (0°, 90° cw, 90° ccw or 180°) as within-subject factors, and group (healthy subjects, left-most affected PD patients or right-most affected PD patients) as a between-subject factor. Finally, following previous studies (Jola & Mast, 2005; Kosslyn et al., 1998), we tested whether the participants used a rotation strategy to mentally transform both body images and letters by performing planned linear contrasts on participants’ correct RTs for the four stimulus orientations, i.e. 0°, 90° cw, 90° ccw, and 180°. This analysis was conducted on each experimental task, separately in the three groups. 3. Results 3.1. Overall performance Pearson’s correlations showed significant negative correlations between overall accuracy and RTs in each group for all experimental tasks (healthy subjects: front-facing-OBT, r = .432, p = .017; back-facing-OBT, r = .456, p = .011; LRT, r = .404, p = .025; left-most affected PD patients: front-facing-OBT, r = .574, p = .032; back-facing-OBT, r = .540, p = .041; LRT, r = .493, p = .045; right-most affected PD patients: front-facing-OBT, r = .528, p = .043; back-facing-OBT, r = .539, p = .031; LRT, r = .574, p = .024). These findings ruled out a trade-off between speed and accuracy (e.g. Sanders, 1998). Patients and healthy subjects performed the three tasks accurately, with mean accuracy and correct RTs comparable across groups (Table 2). The two-way mixed ANOVA performed on accuracy showed a significant effect of task, F(2,112) = 35.708, p = .0001, g2p = .389, with higher accuracy for back-facing-OBT (mean = .92, SEM = .01) and LRT (mean = .91, SEM = .02) relative to front-facingOBT (mean = .79, SEM = .02). The effect of group, F(2,56) = .732, p = .485, g2p = .025, and the task by group interaction, F(4,112) = .336, p = .853, g2p = .012, were not significant. An analogous pattern was obtained by applying the same ANOVA on correct RTs, with a significant effect of task, F(2,112) = 92.126, p = .0001, g2p = .622, with faster RTs for back-facing-OBT (mean = 2522.86, SEM = 72.64) and LRT (mean = 2087.82, SEM = 49.52) relative to front-facing-OBT (mean = 3138.87, SEM = 86.04). The effect of group, F(2,56) = .051, p = .950, g2p = .002, and the task by group interaction, F(4,112) = 1.355, p = .254, g2p = .046, were not significant. 3.2. Effect of patients’ most affected side on whole-body transformation The four-way mixed-design ANOVA performed on correct RTs showed significant effects of task, F(1,56) = 48.793, p = .0001, g2p = .466, with faster RTs in the back-facing-OBT (mean = 2561.06,
Table 2 Mean accuracy and RTs (SEM) of healthy subjects, left-most affected and right-most affected PD patients, separately for the three experimental tasks. Healthy subjects
Left-most affected PD
Right-most affected PD
Mean
Mean
Mean
SEM
SEM
SEM
Accuracy Front-facing-OBT Back-facing-OBT LRT
.80 .95 .91
.03 .01 .01
.78 .90 .92
.04 .02 .02
.76 .93 .90
.04 .02 .02
RTs Front-facing-OBT Back-facing-OBT LRT
3185.61 2415.95 2093.28
122.42 101.66 70.54
3061.14 2638.22 2117.61
179.20 148.81 103.26
3117.94 2629.02 2049.10
173.13 143.77 99.75
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SEM = 76.85) than in front-facing-OBT (mean = 3121.56, SEM = 92.54), and of spatial orientation, with slower RTs for 180° oriented bodies (mean = 3154.94, SEM = 85.96) with respect to the other orientations (0°: mean = 2739.35, SEM = 84.92; 90° cw: mean = 2756.32, SEM = 94.95; 90° ccw: mean = 2714.64, SEM = 84.29). There was a significant first-order interaction between task and spatial orientation, F(3,168) = 8.319, p = .0001, g2p = .129, showing that the influence of stimulus orientation on RTs was different in the OBT tasks (see below analysis of the effect of stimulus orientation on mental transformation). More relevant here, there was a significant first-order interaction between side of marked hand and group, F(2,56) = 3.548, p = .035, g2p = .112, that was further qualified by the significant second-order interaction among task, side of marked hand and group, F(2,56) = 3.939, p = .025, g2p = .123. All remaining main effects and interactions were not significant (p > .05). Post-hoc comparisons (paired t-tests) on the interaction among task, side of marked hand and group (Fig. 2, upper row) showed that the side of marked hand did not affect RTs of the three groups on front-facing-OBT (healthy subjects: t = .114, p = .910; left-most affected PD patients: t = .046, p = .964; right-most affected PD patients: t = .090, p = .929), whereas it specifically modulated performance of both left- and right-most affected PD groups on back-facing-OBT. More precisely, while leftmost affected PD patients were slower in judging back-facing-bodies with left than right marked hand (t = 3.321, p = .006), the opposite was true for right-most affected PD patients (t = 2.774, p = .028); healthy subjects’ RTs, instead, did not differ between left and right marked hand (t = 1.042, p = .306).
Fig. 2. Mean RTs and accuracy (bars are SEM) of the three groups on front-facing-OBT and back-facing-OBT plotted against the side of the figure’s marked hand.
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Fig. 3. Mean RTs (bars are SEM) of the three groups on front-facing-OBT, back-facing-OBT and LRT plotted against the four stimulus orientations.
The same four-way mixed-design ANOVA as above was performed on accuracy and showed a significant main effect of task, F(1,56) = 45.530, p = .0001, g2p = .448, with higher accuracy in the backfacing-OBT (mean = .92, SEM = .01) than in front-facing-OBT (mean = .79, SEM = .02), whereas no other main effect or interaction was significant (p > .05). However, it is worth underlining here that, consistent with RTs, left-most affected PD patients were less accurate in judging back-facing-bodies with left than right marked hand, whereas the opposite was true for right-most affected PD patients. This pattern was absent in healthy participants and in the performance of the three groups on the front-facing-OBT (Fig. 2, lower row). 3.3. Effect of stimulus orientation on mental transformation tasks Fig. 3 shows RTs of the three groups on front-facing-OBT, back-facing-OBT and LRT plotted against the four stimulus orientations. Planned linear contrasts on front-facing-OBT showed that in all the three groups RTs did not increase with increasing stimulus orientation (healthy subjects, F(1,29) = .048, p = .828, g2p = .002; left-most affected PD patients, F(1,13) = 1.274, p = .279, g2p = .089; right-most affected PD patients, F(1,14) = .378, p = .548, g2p = .026). The same analysis on back-facing OBT showed that the linear trend was highly significant in all the three groups (healthy subjects, F(1,29) = 37.625, p = .0001, g2p = .565; left-most affected PD patients, F(1,13) = 46.527, p = .0001, g2p = .782; right-most affected PD patients, F(1,14) = 15.097, p = .002, g2p = .519). However, results showed that quadratic and cubic trends were also significant in healthy subjects (quadratic trend, F(1,29) = 21.267, p = .0001, g2p = .423; cubic trend, F(1,29) = 12.848, p = .001, g2p = .307), and that the quadratic trend was significant in both PD groups (left-most affected PD patients: F(1,13) = 4.794, p = .048, g2p = .198; right-most affected PD patients: F(1,14) = 11.859, p = .004, g2p = .459). On the contrary, planned linear contrasts on LRT showed a clear, significant linear trend in all the three groups (healthy subjects, F(1,29) = 74.666, p = .0001, g2p = .720; left-most affected PD patients, F(1,13) = 21.213, p = .0001, g2p = .620; right-most affected PD patients, F(1,14) = 29.395, p = .0001, g2p = .677), without any other significant trend. 4. Discussion We assessed PD patients on OBT tasks in order to investigate the contribution of embodied simulation to mental transformation of whole-body. To this aim, we tested whether patients’ most affected side influenced the ability to mentally manipulate whole-body images. The results demonstrated that PD patients were specifically impaired in judging laterality of the hand corresponding to their own most affected side when presented with back-facing human figures (back-facing-OBT). The correspondence between the most affected side and mental transformation performance was not found for
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judgments on the human figure presented in a front view (front-facing-OBT). Nonetheless, overall performance of both left- and right-most affected PD patients on OBT and LRT was comparable to that of healthy subjects, although healthy participants were substantially younger and better educated than PD patients. The present data were obtained from the analysis of responses that participants provided with their right dominant hand. Measuring RTs in PD patients can be problematic because of the motor symptoms of the disease (Amick et al., 2006), but in particular our methodological choice might have biased the results because some PD patients responded with their most affected hand, whereas others responded with their least affected hand. However, if this was the case, we should have found that the right-most affected PD patients were slower than left-most affected patients, but we did not find any main effect of the group on RTs in any experimental task or condition. Moreover, as reported above, we also found that mean accuracy was comparable across groups in the three experimental tasks, and the pattern of accuracy data strongly overlapped with RTs on both front- and back-facing OBT. Consistently with previous studies on hand laterality judgments (Helmich et al., 2007; van Nuenen et al., 2012), these findings would rule out a general response bias related to the side of the response hand, and allowed us to interpret data in the framework of embodied simulation mechanisms. Previous studies on healthy subjects revealed some behavioral differences between performance on back- and front-facing-OBT. In particular, it has been repeatedly demonstrated that judgments on a human figure presented in a front view perspective take considerably longer (and are more error prone) than when the body image is shown in back view. Moreover, degree of rotation angle often affects RTs for back view stimuli but not for front view stimuli (e.g., Jola & Mast, 2005; Parsons, 1987b; Steggemann, Engbert, & Weigelt, 2011). Accordingly, in the present study both PD patients and healthy subjects showed: (i) faster (and more accurate) judgments on back- than front-facing-OBT, and (ii) an influence of rotation angle on RTs in back-facing-OBT and letter rotation, but not in front-facingOBT. In the LRT we found a linear increase of RTs with increasing stimulus orientation in both patients and healthy subjects, consistent with classical studies on mental rotation of non-corporeal stimuli (Cooper & Shepard, 1973; Fischer & Pellegrino, 1988). On the contrary, in back-facing-OBT we observed a more complex pattern of relationships between spatial orientation and RTs, suggesting that non-rotational components could have affected whole-body transformation. Zacks, Mires, Tversky, and Hazeltine (2002) hypothesized that non-linear relationships between orientation and RTs when processing whole-bodies could reflect constraints arising from the kinematics of the body. Here, the influence of the PD patients’ most-affected side when processing back-facing stimuli supported the involvement of embodied simulation processes in mental transformation of back-facing whole-bodies. Recently, Gardner and Potts (2010) required right- and left-handed healthy subjects to perform the classical OBT task. Results showed that left-handers were faster in judging the left side, whereas right-handers were faster in judging the right side of the image. These data suggested that embodied simulation might contribute to whole-body transformation in the absence of actual or implied actions (Gardner & Potts, 2010). Moreover, Steggemann et al. (2011) required healthy participants with or without motor expertise for rotational movements to perform back-facing- and front-facing-OBT. Results demonstrated an advantage (shorter RTs and higher accuracy) in making judgments on back- than front-facing human figures independently from motor expertise. Steggemann et al. (2011) suggested that to solve the back-facing-OBT, participants simply had to mentally ‘‘take a step forward’’ to imagine themself into the position of the person presented. On the contrary, mental transformation of front-facing bodies would imply a turn around the longitudinal body axis, likely involving complex visuospatial perspective processes. This interpretation fits well with the present data showing an effect of Parkinson’s disease on cognitive performance in the back- but not in the front-facing-OBT. Thus, two kinds of mental transformations seems to be involved in whole-body processing: an ‘‘embodied transformation’’, that implies simulation of one’s own body movements and is mainly activated when dealing with a back-facing body; and a ‘‘perspective transformation’’, that does not necessarily implies simulation processes and is mainly activated when observing a front-facing body (see also Gardner et al., 2013; Kessler & Thomson, 2010; Kessler & Wang, 2012). This interpretation is consistent with the distinction between embodied and visuospatial transformation mechanisms hypothesized for mental transformation of body-parts (Brady, Maguinness, & Ní Choisdealbha, 2011; Conson, Mazzarella, & Trojano, 2009; Ní Choisdealbha, Brady, &
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Maguinness, 2011). Two recent neurofunctional studies on mental transformation of hand images in right-most affected PD patients (Helmich et al., 2007; van Nuenen et al., 2012) found that the patients’ failure in judging images of the affected hand was related to an increased compensatory activity in the right extrastriate body area. On this basis, the present results would prompt further investigation aimed at verifying whether this compensatory mechanism is also involved in wholebody mental transformation in PD, and whether it changes over the course of the disease. 5. Conclusions Here we demonstrated that the side of stronger motor impairment in PD patients can selectively affect whole-body mental transformations. We found comparable patterns of performance in PD patients and in healthy subjects on front-facing-OBT task and on LRT, consistent with evidence of unimpaired visuospatial transformations in this clinical population (Amick et al., 2006; Dominey et al., 1995). On the contrary, left- and right-most affected PD patients showed opposite patterns of impaired performance on the back-facing-OBT. These findings demonstrated that one’s own body representation is causatively involved in processing whole-bodies, but only when the posture of the body image (i.e., back-facing) activates embodied simulation processes. Acknowledgments We are grateful to Italia Pagano and Daniela Culiers for their help in collecting the data. References American Psychiatric Association (1994). Diagnostic and statistical manual of mental disorders (4th ed. (DSMIV)). Washington, DC: American Psychiatric Association. Amick, M. M., Schendan, H. E., Ganis, G., & Cronin-Golomb, A. (2006). Frontostriatal circuits are necessary for visuomotor transformation: Mental rotation in Parkinson’s disease. Neuropsychologia, 44, 339–349. Arzy, S., Mohr, C., Michel, C., & Blanke, O. (2007). 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Contents lists available at ScienceDirect
Human Movement Science journal homepage: www.elsevier.com/locate/humov
The role of embodied simulation in mental transformation of whole-body images: Evidence from Parkinson’s disease Massimiliano Conson a,⇑, Luigi Trojano a,b, Carmine Vitale c,d, Elisabetta Mazzarella e, Roberto Allocca f, Paolo Barone c,g, Dario Grossi a, Gabriella Santangelo a,c,⇑ a
Neuropsychology Laboratory, Department of Psychology, Second University of Naples, Viale Ellittico 31, 81100 Caserta, Italy Salvatore Maugeri Foundation, IRCCS Institute of Telese Terme (BN), Italy IDC ‘‘Hermitage-Capodimonte’’, Naples, Italy d University of Naples Parthenope, Naples, Italy e Department of Neuromotor Physiology, Scientific Institute Foundation Santa Lucia, Via Ardeatina 306, 00179 Rome, Italy f Department of Neurological Sciences, University Federico II, Naples, Italy g Neurodegenerative Diseases Center, University of Salerno, Salerno, Italy b c
a r t i c l e
i n f o
Article history: Available online 26 November 2013 PsycINFO classification: 2520 Neuropsychology & Neurology Keywords: Embodied cognition Action simulation Mental transformation Parkinson’s disease Mental rotation Motor imagery
a b s t r a c t It has been repeatedly demonstrated that mentally performing an action and mentally transforming body-parts entail simulation of one’s own body movements, consistent with predictions of embodied cognition theories. However, the involvement of embodied simulation in mental transformation of whole-body images is still disputed. Here, we assessed own body transformation in Parkinson’s disease (PD) patients with symptoms most affecting the left or the right body side. PD patients were required to perform left– right judgments on front-facing or back-facing human figures, and a letter rotation task. Results demonstrated that PD patients were selectively impaired in judging the side of back-facing human figures corresponding to their own most affected side, but performed as well as healthy subjects on mental transformation of front-facing bodies and on letter rotation. These findings demonstrate a parallel impairment between motor and mental simulation mechanisms in PD patients, thus highlighting the specific contribution of embodied cognition to mental transformation of whole-body images. Ó 2014 Published by Elsevier B.V.
⇑ Corresponding authors at: Neuropsychology Laboratory, Department of Psychology, Second University of Naples, Viale Ellittico 31, 81100 Caserta, Italy. Tel.: +39 0823 275327. E-mail addresses: [email protected] (M. Conson), [email protected] (G. Santangelo). 0167-9457/$ - see front matter Ó 2014 Published by Elsevier B.V. http://dx.doi.org/10.1016/j.humov.2013.10.006
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1. Introduction Classical psychophysical studies showed that when healthy participants have to judge whether a hand image with a specific spatial orientation is left or right (i.e., the hand laterality task) they imagine their own hand moving to match the stimulus orientation for responding (Parsons, 1987a, 1994; Sekiyama, 1982). Moreover, making hand laterality judgments and executing a hand movement follow the same temporal profile and the same hand-specific joint-constraints (Conson, Mazzarella, & Trojano, 2011; de Lange, Helmich, & Toni, 2006; Parsons, 1987a, 1994; Sekiyama, 1982). Accordingly, specific impairments on the hand laterality task and spared mental transformation of object images have been reported in patients with severe motor disorders, such as locked-in syndrome (Conson, Pistoia, Sarà, Grossi, & Trojano, 2010; Conson et al., 2008), amyotrophic lateral sclerosis (Fiori et al., 2013a) or spinal cord injury (Fiori et al., 2013b). These observations consistently support the model of embodied cognition according to which cognitive processes are grounded in bodily states (Gallese & Sinigaglia, 2011). In this view, the same sensorimotor representations activated when performing an actual action are also involved in different ‘‘action-related phenomena’’ such as motor imagery (i.e., mental simulation of body-parts movements), action observation and imitation (Decety & Grèzes, 2006; Gallese & Sinigaglia, 2011; Jeannerod, 2001). No clear data are available instead on the role of embodied simulation in mental transformation of whole-body images. In a seminal neuroimaging study, Zacks, Rypma, Gabrieli, Tversky, and Glover (1999) presented participants with front-facing or back-facing schematic human figures with one outstretched arm; in order to judge which arm was outstretched (i.e., left–right judgment), participants imagined themselves in the position of the figure. This own body transformation led to increased cortical activity in the temporo-parietal junction, as well as in other areas including the frontal cortex. Subsequent neurofunctional studies employing the same paradigm (Arzy, Mohr, Michel, & Blanke, 2007; Arzy, Thut, Mohr, Michel, & Blanke, 2006; Blanke et al., 2005) confirmed the involvement of the temporo-parietal junction in whole-body processing and suggested that whole-body transformations imply some sort of ‘‘rotation of the self’’ (Arzy et al., 2006, 2007; Blanke et al., 2005). This evidence would suggest that, analogously to body-parts transformation, mental transformation of whole-body is grounded on embodied cognitive processes (Kessler & Thomson, 2010). However, other studies demonstrated that whole-body transformation can also be accomplished by resorting to an object-based, visuospatial transformation not related to one’s own body representation (Gardner, Brazier, Edmonds, & Gronholm, 2013; Kessler & Wang, 2012). For instance, Kessler and Wang (2012) reported that healthy individuals with low empathic abilities were more prone to rely on object rotation strategies to solve the own body transformation task. These findings would undermine the idea that whole-body transformation is dependent on actual sensorimotor information available in the agent’s brain. In synthesis, the role of embodied simulation in whole-body transformation is not supported consistently. Strong clues on this issue could be provided by a behavioral study on patients with a welldefined damage of the motor system, such as Parkinson’s disease (PD). Neuropsychological studies investigating mental transformation of body-parts in PD patients by means of the hand laterality task reported motor imagery asymmetries: patients mentally simulated movements more slowly with their most affected hand (Amick, Schendan, Ganis, & Cronin-Golomb, 2006; Dominey, Decety, Broussolle, Chazot, & Jeannerod, 1995). These results were confirmed by recent experiments in which PD patients performed the hand laterality task while keeping their arms in different postures (Helmich, de Lange, Bloem, & Toni, 2007; van Nuenen et al., 2012). Taken together, available evidence supported the strong relationships between motor disorders and mental transformation of body-parts in PD patients. However, no evidence is available about mental transformation of whole-body images in this clinical population. In the present study we required PD patients to perform own body transformation tasks requiring laterality judgments on a schematic human figure. If sensorimotor information is causatively involved in processing of whole-bodies, we can predict that PD patients would be impaired on own body transformation task, and that the side of motor impairment would affect behavioral performance, with opposite patterns in patients with left or right most affected side. More precisely, consistent with previous studies on mental transformation of body parts (Helmich et al., 2007; van Nuenen et al., 2012),
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we could expect that PD patients are specifically impaired in judging the body side corresponding to their own most affected side. Relevant here, we also assessed PD patients’ ability to perform mental rotation of letters that is thought not to involve one’s own body representation (Conson et al., 2008, 2010; Dalecki, Hoffmann, & Bock, 2012; Fiori et al., 2013a, 2013b; Kosslyn, Di Girolamo, Thompson, & Alpert, 1998). By these means we could ascertain whether any failure in own body transformation was associated with a generalized deficit in performing mental transformation tasks. 2. Material and methods 2.1. Participants We screened consecutive PD patients attending the Movement Disorders Unit of the University of Naples Federico II (Naples, Italy) from February to June 2012. Patients were enrolled in the study if they met the following inclusion criteria: diagnosis of idiopathic PD according to United Kingdom Parkinson’s Disease Society brain bank (Gibb & Lees, 1988); clinical and history evidence of asymmetric motor disturbances; lack of PD-associated dementia (PDD) as diagnosed according to an algorithm for clinical diagnosis of PDD recommended by the MDS Task Force (Emre et al., 2007); lack of major depression according to DSM IV criteria (American Psychiatric Association, APA, 1994). All PD patients underwent a neurological examination including the Unified Parkinson’s Disease Rating Scale motor subscale (UPDRS-III; Fahn, Elton, & Members of the UPDRS Development Committee, 1987) to evaluate severity of motor symptoms, and Hoehn & Yahr Scale (H&Y; Hoehn & Yahr, 1967) to assess PD stage. Age, level of formal education, age at onset, side of onset of PD, disease duration, and type and dosage of pharmacological treatment were recorded; Levodopa equivalent daily dose (LEDD) was calculated (Tomlinson et al., 2010). As a screening for general cognitive impairment we used an Italian version of the Mini Mental State Examination (MMSE), and excluded from the study PD patients with a total age- and educational-adjusted score <23.8, that is the standard cut-off for the normal range (Folstein, Folstein, & McHugh, 1975; Measso et al., 1993). Twenty-nine right-handed patients (10 females and 19 males) matched inclusion and exclusion criteria. Mean patients’ age was 67.6 ± 7.7 years (range 54–83 years) and mean educational level was 10.9 ± 4.9 (range 3–18 years). In the total sample, mean age at onset was 60.7 ± 8.5 (range 44–77 years) and mean disease duration was 7 ± 4.3 years (range 2–21 years), respectively. Mean UPDRS-III scores were 14.1 ± 4.9 (range 6–28). H&Y rating scale ranged from Stage I to Stage III. Mean total LEDD was 621.5 ± 295.6 mg (range 150–1300). Side of onset of motor symptoms and of most severe motor disturbances on repeated clinical assessment (most affected side) was the left in 14/29 patients (left-most affected PD: 48.3%) and the right in 15/29 (right-most affected PD: 51.7%) patients. No significant differences between the two groups were found on demographic and clinical features (Table 1). PD patients underwent the experimental tasks (see below) when they were in the ‘‘on’’ phase. Thirty right-handed healthy subjects (10 females and 20 males; mean age 49.7 years, SD 7.3, range 46–83 years; mean education 14.7, SD 2.5, range 11–18 years) took part in the experiment as healthy controls. Exclusion criteria were the following: (1) diagnosis of PD or any other neurologic or psychiatric disorder; (2) clinically evident dementia or major depression, both diagnosed by means of DSM IV criteria (APA, 1994); (3) general intellectual impairment, defined by MMSE score below the normal cut-off, as above. The study was conducted in accordance with the ethical standards of Helsinki Declaration and an informed consent was obtained from all participants after the nature of the study was fully explained to them. 2.2. Experimental tasks Participants underwent the classical own body transformation task (OBT; Arzy et al., 2006; Blanke et al., 2005; Parsons, 1987b; Zacks et al., 1999), requiring left–right judgments on a human image whose left or right hand was marked to appear as wearing a black glove. After imagining themselves to be in the figure’s body position and to have its visual perspective, participants had to judge whether
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Table 1 Mean (±SD) of demographic and clinical features of PD patients.
Age (yr) Education (yr) Sex (M/F) Age at PD onset (yr) PD duration (yr) UPDRS-III score in on-state H&Y score Total-LEDD (mg/d) Dopamine agonist LEDD (mg/d) Patients receiving levodopa monotherapy Patients receiving dopamine agonist monotherapy Patients receiving combination agonist and levodopa therapy
Left-most affected PD (n = 14)
Right-most affected PD (n = 15)
F/U test
P
62.9 ± 4.7 10.8 ± 5.8 8/6 61.8 ± 8.4 7.5 ± 5.1 12.9 ± 4.1 1.9 ± 0.6 626.8 ± 328.5 483.3 ± 360.5 5 3 6
66 ± 8.6 11 ± 4.8 11/4 59.7 ± 8.7 6.6 ± 3.5 15.4 ± 5.6 1.7 ± 0.6 616.7 ± 278 340 ± 218.1 2 2 11
1.347 .015 .840 .442 .310 1.767 93 .008 1.490
.256 .904 .359 .512 .582 .195 .621 .929 .235
Yr = years; PD = Parkinson’s disease; UPDRS-III = Unified Parkinson’s disease rating scale; H&Y = Hohen & Yahr; Total LEDD = Total L-Dopa equivalent daily dose.
the left or the right hand of the human figure was marked. Human images were displayed facing toward (front-facing-OBT) or away from the observers (back-facing-OBT). The back-facing orientation is compatible with the participants’ perspective, whereas in the front-facing orientation the observers have to imagine their own bodies into the position of the front-facing human figure to perform the left/right judgment. Following previous studies (Arzy et al., 2006; Blanke et al., 2005; Zacks et al., 1999), task instructions explicitly required participants to mentally simulate one’s own body movement. By these means, we could induce subjects to resort to one’s own body representation during task performance (see Hétu et al., 2013, for a discussion on explicit versus implicit motor imagery). Participants also completed a letter rotation task (LRT), requiring whether a capital letter was presented in canonical or mirror-reversed form (Conson et al., 2008). The three tasks (i.e. front-facingOBT, back-facing-OBT and LRT) were administered by means of a computerized procedure, and were arranged to be as similar as possible in presentation and response modalities, although specific instructions differed.
2.3. Stimuli and procedure Stimuli consisted of line drawings depicting front-facing or back-facing body images whose right or left hand was marked in black, or of letters in canonical or mirror-reversed form. All stimuli were presented in four spatial orientations: 0°, 90° clockwise (cw), 90° counterclockwise (ccw) and 180° (Fig. 1). Stimuli were large approximately 8 cm along the widest axis (about 7.6° of visual angle at a viewing distance of 60 cm from a 15’’ computer screen) and were presented at the centre of the monitor until response completion; each stimulus was preceded by a fixation point (1000 ms). Patients and healthy controls gave their responses by pressing one of two centrally located keys (B and H keys on QWERTY keyboard) with their index and middle fingers of the right (dominant) hand; the stimulus-response association for each task was counterbalanced across participants. The left hand was placed in a comfortable position, palm down next to the keyboard. Following classical studies (e.g., Sekiyama, 1982), both hands were covered with a black cloth in order to avoid that visual cues provided by one’s own hands could facilitate left–right judgments on body images (for instance see Ionta & Blanke, 2009 for recent data on the role of visual familiarity on mental transformation of body-parts). Participants were encouraged to respond as fast and correctly as possible; we recorded both Reaction Times (RTs, in milliseconds) and accuracy. Stimulus presentation and data collection were controlled by a PC using Cedrus SuperLab v.4. Each task (front-facing-OBT, back-facing-OBT and LRT) consisted of 48 trials: in both front-facingand back-facing-OBT, six trials were presented for each combination of hand laterality (left or right)
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Fig. 1. Instances of stimuli used in the three mental transformation tasks: front-facing-OBT (first row), back-facing-OBT (second row), and letter rotation task (LRT, third row), in the four spatial orientations: 0°, 90° clockwise (cw), 90° counterclockwise (ccw) and 180° (schematic human figures with their left hand marked in black, and letters in mirror-reversed form are not reported here).
and spatial orientation; in the LRT, six trials were presented for each combination of type of stimulus (canonical or mirror-reversed) and spatial orientation. Trials were randomized within each task, which was divided in two blocks, with a 3-min pause allowed between the two blocks. A training period preceded the experiment. Before starting each task, eight practice trials were given; if a wrong response was provided, feedback appeared on the monitor screen and the trial was repeated. Experimental session started only if the participants provided at least six consecutive correct responses. Testing was conducted in a quiet room and in a single session that lasted about 20 min; the order of the three tasks was counterbalanced across participants. 2.4. Statistical analysis First, Pearson’s correlations between accuracy and RTs were calculated for each mental rotation task in each group to assess whether participants’ performance showed any speed-accuracy tradeoff (Sanders, 1998). Then, overall mean RTs and accuracy were analyzed by means of separate twoway mixed Analysis of Variance (ANOVA), with task (front-facing-OBT, back-facing-OBT and LRT) as a within-subject factor and with group (healthy participants, left-most affected and right-most affected PD patients) as a between-subject factor.
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To ascertain the involvement of embodied processing in whole-body transformation, we tested whether the side of prevalent motor impairment in PD patients specifically affected performance on the corresponding side of the human figure in the OBT tasks. To this aim, a four-way mixed-design ANOVA was performed on correct RTs and accuracy, with task (front-facing-OBT or back-facing-OBT), side of marked hand (left or right) and spatial orientation (0°, 90° cw, 90° ccw or 180°) as within-subject factors, and group (healthy subjects, left-most affected PD patients or right-most affected PD patients) as a between-subject factor. Finally, following previous studies (Jola & Mast, 2005; Kosslyn et al., 1998), we tested whether the participants used a rotation strategy to mentally transform both body images and letters by performing planned linear contrasts on participants’ correct RTs for the four stimulus orientations, i.e. 0°, 90° cw, 90° ccw, and 180°. This analysis was conducted on each experimental task, separately in the three groups. 3. Results 3.1. Overall performance Pearson’s correlations showed significant negative correlations between overall accuracy and RTs in each group for all experimental tasks (healthy subjects: front-facing-OBT, r = .432, p = .017; back-facing-OBT, r = .456, p = .011; LRT, r = .404, p = .025; left-most affected PD patients: front-facing-OBT, r = .574, p = .032; back-facing-OBT, r = .540, p = .041; LRT, r = .493, p = .045; right-most affected PD patients: front-facing-OBT, r = .528, p = .043; back-facing-OBT, r = .539, p = .031; LRT, r = .574, p = .024). These findings ruled out a trade-off between speed and accuracy (e.g. Sanders, 1998). Patients and healthy subjects performed the three tasks accurately, with mean accuracy and correct RTs comparable across groups (Table 2). The two-way mixed ANOVA performed on accuracy showed a significant effect of task, F(2,112) = 35.708, p = .0001, g2p = .389, with higher accuracy for back-facing-OBT (mean = .92, SEM = .01) and LRT (mean = .91, SEM = .02) relative to front-facingOBT (mean = .79, SEM = .02). The effect of group, F(2,56) = .732, p = .485, g2p = .025, and the task by group interaction, F(4,112) = .336, p = .853, g2p = .012, were not significant. An analogous pattern was obtained by applying the same ANOVA on correct RTs, with a significant effect of task, F(2,112) = 92.126, p = .0001, g2p = .622, with faster RTs for back-facing-OBT (mean = 2522.86, SEM = 72.64) and LRT (mean = 2087.82, SEM = 49.52) relative to front-facing-OBT (mean = 3138.87, SEM = 86.04). The effect of group, F(2,56) = .051, p = .950, g2p = .002, and the task by group interaction, F(4,112) = 1.355, p = .254, g2p = .046, were not significant. 3.2. Effect of patients’ most affected side on whole-body transformation The four-way mixed-design ANOVA performed on correct RTs showed significant effects of task, F(1,56) = 48.793, p = .0001, g2p = .466, with faster RTs in the back-facing-OBT (mean = 2561.06,
Table 2 Mean accuracy and RTs (SEM) of healthy subjects, left-most affected and right-most affected PD patients, separately for the three experimental tasks. Healthy subjects
Left-most affected PD
Right-most affected PD
Mean
Mean
Mean
SEM
SEM
SEM
Accuracy Front-facing-OBT Back-facing-OBT LRT
.80 .95 .91
.03 .01 .01
.78 .90 .92
.04 .02 .02
.76 .93 .90
.04 .02 .02
RTs Front-facing-OBT Back-facing-OBT LRT
3185.61 2415.95 2093.28
122.42 101.66 70.54
3061.14 2638.22 2117.61
179.20 148.81 103.26
3117.94 2629.02 2049.10
173.13 143.77 99.75
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SEM = 76.85) than in front-facing-OBT (mean = 3121.56, SEM = 92.54), and of spatial orientation, with slower RTs for 180° oriented bodies (mean = 3154.94, SEM = 85.96) with respect to the other orientations (0°: mean = 2739.35, SEM = 84.92; 90° cw: mean = 2756.32, SEM = 94.95; 90° ccw: mean = 2714.64, SEM = 84.29). There was a significant first-order interaction between task and spatial orientation, F(3,168) = 8.319, p = .0001, g2p = .129, showing that the influence of stimulus orientation on RTs was different in the OBT tasks (see below analysis of the effect of stimulus orientation on mental transformation). More relevant here, there was a significant first-order interaction between side of marked hand and group, F(2,56) = 3.548, p = .035, g2p = .112, that was further qualified by the significant second-order interaction among task, side of marked hand and group, F(2,56) = 3.939, p = .025, g2p = .123. All remaining main effects and interactions were not significant (p > .05). Post-hoc comparisons (paired t-tests) on the interaction among task, side of marked hand and group (Fig. 2, upper row) showed that the side of marked hand did not affect RTs of the three groups on front-facing-OBT (healthy subjects: t = .114, p = .910; left-most affected PD patients: t = .046, p = .964; right-most affected PD patients: t = .090, p = .929), whereas it specifically modulated performance of both left- and right-most affected PD groups on back-facing-OBT. More precisely, while leftmost affected PD patients were slower in judging back-facing-bodies with left than right marked hand (t = 3.321, p = .006), the opposite was true for right-most affected PD patients (t = 2.774, p = .028); healthy subjects’ RTs, instead, did not differ between left and right marked hand (t = 1.042, p = .306).
Fig. 2. Mean RTs and accuracy (bars are SEM) of the three groups on front-facing-OBT and back-facing-OBT plotted against the side of the figure’s marked hand.
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Fig. 3. Mean RTs (bars are SEM) of the three groups on front-facing-OBT, back-facing-OBT and LRT plotted against the four stimulus orientations.
The same four-way mixed-design ANOVA as above was performed on accuracy and showed a significant main effect of task, F(1,56) = 45.530, p = .0001, g2p = .448, with higher accuracy in the backfacing-OBT (mean = .92, SEM = .01) than in front-facing-OBT (mean = .79, SEM = .02), whereas no other main effect or interaction was significant (p > .05). However, it is worth underlining here that, consistent with RTs, left-most affected PD patients were less accurate in judging back-facing-bodies with left than right marked hand, whereas the opposite was true for right-most affected PD patients. This pattern was absent in healthy participants and in the performance of the three groups on the front-facing-OBT (Fig. 2, lower row). 3.3. Effect of stimulus orientation on mental transformation tasks Fig. 3 shows RTs of the three groups on front-facing-OBT, back-facing-OBT and LRT plotted against the four stimulus orientations. Planned linear contrasts on front-facing-OBT showed that in all the three groups RTs did not increase with increasing stimulus orientation (healthy subjects, F(1,29) = .048, p = .828, g2p = .002; left-most affected PD patients, F(1,13) = 1.274, p = .279, g2p = .089; right-most affected PD patients, F(1,14) = .378, p = .548, g2p = .026). The same analysis on back-facing OBT showed that the linear trend was highly significant in all the three groups (healthy subjects, F(1,29) = 37.625, p = .0001, g2p = .565; left-most affected PD patients, F(1,13) = 46.527, p = .0001, g2p = .782; right-most affected PD patients, F(1,14) = 15.097, p = .002, g2p = .519). However, results showed that quadratic and cubic trends were also significant in healthy subjects (quadratic trend, F(1,29) = 21.267, p = .0001, g2p = .423; cubic trend, F(1,29) = 12.848, p = .001, g2p = .307), and that the quadratic trend was significant in both PD groups (left-most affected PD patients: F(1,13) = 4.794, p = .048, g2p = .198; right-most affected PD patients: F(1,14) = 11.859, p = .004, g2p = .459). On the contrary, planned linear contrasts on LRT showed a clear, significant linear trend in all the three groups (healthy subjects, F(1,29) = 74.666, p = .0001, g2p = .720; left-most affected PD patients, F(1,13) = 21.213, p = .0001, g2p = .620; right-most affected PD patients, F(1,14) = 29.395, p = .0001, g2p = .677), without any other significant trend. 4. Discussion We assessed PD patients on OBT tasks in order to investigate the contribution of embodied simulation to mental transformation of whole-body. To this aim, we tested whether patients’ most affected side influenced the ability to mentally manipulate whole-body images. The results demonstrated that PD patients were specifically impaired in judging laterality of the hand corresponding to their own most affected side when presented with back-facing human figures (back-facing-OBT). The correspondence between the most affected side and mental transformation performance was not found for
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judgments on the human figure presented in a front view (front-facing-OBT). Nonetheless, overall performance of both left- and right-most affected PD patients on OBT and LRT was comparable to that of healthy subjects, although healthy participants were substantially younger and better educated than PD patients. The present data were obtained from the analysis of responses that participants provided with their right dominant hand. Measuring RTs in PD patients can be problematic because of the motor symptoms of the disease (Amick et al., 2006), but in particular our methodological choice might have biased the results because some PD patients responded with their most affected hand, whereas others responded with their least affected hand. However, if this was the case, we should have found that the right-most affected PD patients were slower than left-most affected patients, but we did not find any main effect of the group on RTs in any experimental task or condition. Moreover, as reported above, we also found that mean accuracy was comparable across groups in the three experimental tasks, and the pattern of accuracy data strongly overlapped with RTs on both front- and back-facing OBT. Consistently with previous studies on hand laterality judgments (Helmich et al., 2007; van Nuenen et al., 2012), these findings would rule out a general response bias related to the side of the response hand, and allowed us to interpret data in the framework of embodied simulation mechanisms. Previous studies on healthy subjects revealed some behavioral differences between performance on back- and front-facing-OBT. In particular, it has been repeatedly demonstrated that judgments on a human figure presented in a front view perspective take considerably longer (and are more error prone) than when the body image is shown in back view. Moreover, degree of rotation angle often affects RTs for back view stimuli but not for front view stimuli (e.g., Jola & Mast, 2005; Parsons, 1987b; Steggemann, Engbert, & Weigelt, 2011). Accordingly, in the present study both PD patients and healthy subjects showed: (i) faster (and more accurate) judgments on back- than front-facing-OBT, and (ii) an influence of rotation angle on RTs in back-facing-OBT and letter rotation, but not in front-facingOBT. In the LRT we found a linear increase of RTs with increasing stimulus orientation in both patients and healthy subjects, consistent with classical studies on mental rotation of non-corporeal stimuli (Cooper & Shepard, 1973; Fischer & Pellegrino, 1988). On the contrary, in back-facing-OBT we observed a more complex pattern of relationships between spatial orientation and RTs, suggesting that non-rotational components could have affected whole-body transformation. Zacks, Mires, Tversky, and Hazeltine (2002) hypothesized that non-linear relationships between orientation and RTs when processing whole-bodies could reflect constraints arising from the kinematics of the body. Here, the influence of the PD patients’ most-affected side when processing back-facing stimuli supported the involvement of embodied simulation processes in mental transformation of back-facing whole-bodies. Recently, Gardner and Potts (2010) required right- and left-handed healthy subjects to perform the classical OBT task. Results showed that left-handers were faster in judging the left side, whereas right-handers were faster in judging the right side of the image. These data suggested that embodied simulation might contribute to whole-body transformation in the absence of actual or implied actions (Gardner & Potts, 2010). Moreover, Steggemann et al. (2011) required healthy participants with or without motor expertise for rotational movements to perform back-facing- and front-facing-OBT. Results demonstrated an advantage (shorter RTs and higher accuracy) in making judgments on back- than front-facing human figures independently from motor expertise. Steggemann et al. (2011) suggested that to solve the back-facing-OBT, participants simply had to mentally ‘‘take a step forward’’ to imagine themself into the position of the person presented. On the contrary, mental transformation of front-facing bodies would imply a turn around the longitudinal body axis, likely involving complex visuospatial perspective processes. This interpretation fits well with the present data showing an effect of Parkinson’s disease on cognitive performance in the back- but not in the front-facing-OBT. Thus, two kinds of mental transformations seems to be involved in whole-body processing: an ‘‘embodied transformation’’, that implies simulation of one’s own body movements and is mainly activated when dealing with a back-facing body; and a ‘‘perspective transformation’’, that does not necessarily implies simulation processes and is mainly activated when observing a front-facing body (see also Gardner et al., 2013; Kessler & Thomson, 2010; Kessler & Wang, 2012). This interpretation is consistent with the distinction between embodied and visuospatial transformation mechanisms hypothesized for mental transformation of body-parts (Brady, Maguinness, & Ní Choisdealbha, 2011; Conson, Mazzarella, & Trojano, 2009; Ní Choisdealbha, Brady, &
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Maguinness, 2011). Two recent neurofunctional studies on mental transformation of hand images in right-most affected PD patients (Helmich et al., 2007; van Nuenen et al., 2012) found that the patients’ failure in judging images of the affected hand was related to an increased compensatory activity in the right extrastriate body area. On this basis, the present results would prompt further investigation aimed at verifying whether this compensatory mechanism is also involved in wholebody mental transformation in PD, and whether it changes over the course of the disease. 5. Conclusions Here we demonstrated that the side of stronger motor impairment in PD patients can selectively affect whole-body mental transformations. We found comparable patterns of performance in PD patients and in healthy subjects on front-facing-OBT task and on LRT, consistent with evidence of unimpaired visuospatial transformations in this clinical population (Amick et al., 2006; Dominey et al., 1995). 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