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Unusual actions do not always trigger the mentalizing network a
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Lisa Ampe , Ning Ma , Nicole Van Hoeck , Marie Vandekerckhove & Frank Van Overwalle
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Department of Psychology, Vrije Universiteit Brussel, Brussels, Belgium Version of record first published: 28 Nov 2012.
To cite this article: Lisa Ampe , Ning Ma , Nicole Van Hoeck , Marie Vandekerckhove & Frank Van Overwalle (2012): Unusual actions do not always trigger the mentalizing network, Neurocase: The Neural Basis of Cognition, DOI:10.1080/13554794.2012.741251 To link to this article: http://dx.doi.org/10.1080/13554794.2012.741251
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NEUROCASE 2012, iFirst, 1–6
Unusual actions do not always trigger the mentalizing network Lisa Ampe, Ning Ma, Nicole Van Hoeck, Marie Vandekerckhove, and Frank Van Overwalle Downloaded by [VUB Vrije University Brussels] at 04:50 28 November 2012
Department of Psychology, Vrije Universiteit Brussel, Brussels, Belgium
Past fMRI research has demonstrated that to understand other people’s behavior shown visually, the mirror network is strongly involved. However, the mentalizing network is also recruited when a visually presented action is unusual and/or when perceivers think explicitly about the intention. To further explore the conditions that trigger mentalizing activity, we replicated one of such studies (de Lange, Spronk, Willems, Toni, & Bekkering, 2008, Current Biology, 18, 454) under the minimal instruction to “view” pictures of unusual actions, without giving any “intention” instruction as in the original study. Contrary to earlier research, merely viewing unusual actions did not activate mentalizing areas. Instead, the dorsal anterior cingulate cortex was activated. We conclude that unusual actions are not sufficient by themselves to trigger mentalizing. In order to activate the mentalizing network without an intention instruction, a richer action context informative of the implausibility of the action might be a prerequisite. Keywords: Unusual action; Mirror network; Mentalizing.
As social beings, people constantly try to make sense of the social world around them and to understand other people’s actions. On the brain level, there is a growing consensus that action understanding may involve two independent networks (cf., meta-analysis by Van Overwalle & Baetens, 2009). First, a mirror network that matches observed behavior to one’s own behavioral repertoire and the goals associated with them, and so allows to understand the goals of others at a basic, perceptual level. Second, a mentalizing network that supports action and goal understanding at a more abstract level through inferential processes, also known as theory of mind.
However, recent evidence suggests that when observable actions are unusual, the mirror network alone seems insufficient for understanding observable actions, and mentalizing areas are also recruited (Van Overwalle & Baetens, 2009). Unusual is defined as actions that do not fit a given context and are thus atypical and unexpected. For example, when people observe actions that are erroneous, pretended or faked, or implausible given physical constraints (Brass, Schmitt, Spengler, & Gergely, 2007; Liepelt, von Cramon, & Brass, 2008). The mentalizing network is also activated during action observation when people think consciously about the intention of an action (Buccino
Address correspondence to Frank Van Overwalle, Department of Psychology, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium. (E-mail:
[email protected]). We are very grateful to Floris de Lange and his colleagues Marjolein Spronk, Roel Willems, Ivan Toni, and Harold Bekkering for providing us with their stimulus material. We would like to thank Floris de Lange in particular, for his valuable feedback on the experimental design. This research was supported by a PhD research Fellowship to the first author from the Research Foundation – Flanders (FWO).
c 2012 Taylor & Francis http://www.tandfonline.com
http://dx.doi.org/10.1080/13554794.2012.741251
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et al., 2007; de Lange, Spronk, Willems, Toni, & Bekkering, 2008; Spunt, Falk, & Lieberman, 2010; Spunt, Satpute, & Lieberman, 2011). However, a few studies did not find mentalizing activity given unusual actions (de Lange et al., 2008; Jastorff, Clavagnier, Gergely, & Orban, 2011; Manthey, Schubotz, & von Cramon, 2003), even when the conditions were quite similar to the other studies mentioned earlier. For instance, de Lange et al. (2008) presented an actor holding various objects at unusual places of the head (e.g., holding a cup at one’s ear instead of in front of one’s mouth) and mentalizing areas were recruited only when instructions were given to judge the intention of the action, not when the means by which the action was carried out had to be judged (e.g., the hand grip holding the cup). Given these conflicting results, the question remains which specific conditions need to be met for unusual actions to trigger the mentalizing network. To explore this issue further, we replicated de Lange et al. (2008) under spontaneous “viewing” rather than explicit instructions to attend to the intention or means of the action. Indeed, it is possible that an instruction to judge the means in the study by de Lange et al. (2008), rather than acting as a neutral condition, may actually have focused the participants’ attention away from the implied intention in atypical behaviors. To avoid such distraction, a “viewing” instruction seems more neutral and may allow for spontaneous mentalizing about intentionality. Based on earlier research, we expect under such spontaneous instruction to replicate the original findings of de Lange et al. (2008). Specifically, we predict activity in the mentalizing network for unusual action intentions (i.e., unusual object locations). In addition, for unusual means (e.g., unusual hand grip), we also predict activity in the extrastriate body area (EBA) and anterior intraparietal sulcus (aIPS; part of the mirror network).
METHOD Participants Twenty healthy participants (16 women and 4 men, mean age = 21.7, age range = 18–27 years), all students at the Ghent University or at the Vrije Universiteit Brussel took part in the experiment. Participants reported no history of neurological, major medical, or psychiatric disorders. Other exclusion criteria were left handedness,
regular taking of medication or drugs and contraindications to fMRI such as pregnancy, claustrophobia, metallic implants, etc. All participants had normal or corrected-to-normal vision. Three additional participants were excluded from further analysis after the experiment; one because of too much body movement in the scanner (more than 10% outlier scans), one because of poor attention to the stimuli (only 24% catch trials correct), and one because of a scanner crash. The experiment was approved by the Medical Ethics Committee at the University Hospital of Ghent and Brussels. Informed consent was obtained from the participants and they received 10 euro for their participation.
Procedure and stimulus material The stimuli and the design were replicated from de Lange et al. (2008). In brief, four types of actions were shown: (i) normal actions (e.g., an actor bringing a coffee cup to her mouth), (ii) actions with an unusual intention (e.g., an actor bringing a coffee cup to her ear), (iii) actions performed with unusual means (e.g., an actor bringing a coffee cup to her mouth while holding the cup with a power grip), and (iv) actions with both an unusual intention and performed with unusual means (e.g., an actor bringing a coffee cup to her ear while holding the cup with a power grip). Participants saw 168 pictures (14 objects each shown while the actor looked in three directions [left–front–right] for four conditions) in a randomized order, each for a duration of 3 s followed by a blank screen for 2 s and a random jitter (0–1 s). After a set of 20 pictures, there was a pause of 35 s (i.e., blank screen with pause message). In contrast to de Lange et al. (2008), there were no explicit instructions to attend to the intention nor to the means of the action. Instead, participants were only instructed to watch the pictures carefully. Moreover, while de Lange et al. (2008) used blocks of 6–7 stimuli (from the same condition) preceded by the instruction, the present study used a random presentation of stimuli. Given the lack of a specific instruction, we included 10% additional pictures as catch trials (i.e., an actor interacting with an earring) to which participants had to react with a button press. All participants in the analysis had 94% or more of the catch trials correct. A pilot study (n = 76) prior to the experiment confirmed that for the 14 objects used under the scanner, actions with an unusual intention (M = 6.70,
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UNUSUAL ACTIONS
SD = 1.74) were perceived as more unusual on a 0–10 scale than actions with an unusual means (M = 4.71, SD = 1.63; t(13) = 3.12, p < .001) or normal actions (M = 1.83, SD = 1.02; t(13) = 9.60, p < .001). Nevertheless, the majority of participants in the pilots were able to come up with at least one goal interpretation of each action (51–100%), although the proportion of goals provided was lower for actions with an unusual intention (M = 77%, SD = 11%) than for actions with an unusual means (M = 92%, SD = 7%; t(13) = 4.04, p < .001) or normal actions (M = 98%, SD = 3%; t(13) = 6.38, p < .001). Imaging procedure Images were collected with a 3-Tesla Magnetom Trio MRI scanner system (Siemens Medical Systems, Erlangen, Germany), using an 8-channel radiofrequency head coil. Stimuli were projected onto a screen at the end of the magnet bore that participants viewed by way of a mirror mounted on the head coil. Stimulus presentation was controlled by E-Prime 2.0 (www.pstnet.com/eprime; Psychology Software Tools) under Windows XP. Immediately prior to the experiment, participants completed a brief practice session. Foam cushions were placed within the head coil to minimize head movements. A high-resolution T1-weighted structural scan (MP-RAGE) was first collected, followed by one functional run of about 770 volume acquisitions (30 axial slices; 4 mm thick; 1 mm skip) of which the first 54 scans for practice trials were omitted. Functional scanning used a gradient-echo echoplanar pulse sequence (TR = 2 s; TE = 33 ms; 3.5 × 3.5 × 4.0 mm in-plane resolution). Image processing and statistical analysis The fMRI data were preprocessed and analyzed using SPM8 (Statistical Parametric Mapping; The Wellcome Trust Centre for NeuroImaging, London, UK). For each functional run, data were preprocessed to remove sources of noise and artifact. Functional data were corrected for differences in acquisition time between slices for each whole-brain volume, realigned within and across runs to correct for head movement, and co-registered with each participant’s anatomical data. Functional data were then transformed into a standard anatomical space (2 mm isotropic voxels) based on the ICBM 152 brain template
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(Montreal Neurological Institute), which approximates Talairach and Tournoux atlas space. Normalized data were then spatially smoothed (6 mm full-width-at-half-maximum – FWHM) using a Gaussian kernel. Additional artifact analysis was performed on the realigned data, using the Artifact Detection Tool software package (ART; http://www.nitrc.org/projects/artifact_detect/), to detect and correct for excessive movement artifacts. Outlier scan movements (identified by assessing between-scan differences with Z-threshold: 3.0, scan to scan movement threshold: 0.5 mm; rotation threshold: 0.02 radians) were omitted in the statistical analysis by including in the general linear model a single regressor for each outlier (i.e., bad scan). No correlations between motion and experimental design or global signal and experimental design were identified. Six directions of motion parameters from the realignment step as well as outlier time points (defined by ART) were included as nuisance regressors. We used a default high-pass filter of 128 s and serial correlations were accounted for by the default auto-regressive AR(1) model. Statistical analyses involved a first-level single participant event-related design with a regressor for each condition time-locked at the presentation of the picture, and additional movement and nuisance artifact regressors, and applying a canonical response function (duration set to 0) using the general linear model of SPM8. Contrasts of interest were performed at the individual first-level using simple t-tests, and then at the group second-level on the parameter estimates (regressors) associated with each first-level contrast. This analysis proved to be more sensitive than a contrast analysis at the second level, using the parameter estimates of each condition. Given the lack of specific instructions, a lenient whole-brain threshold of p ≤ .005 (uncorrected) was used for all comparisons with a cluster extent of 10 voxels (see also Ma, Vandekerckhove, Van Overwalle, Seurinck, & Fias, 2011). Statistical comparisons between conditions of interest are reported after correction for multiple comparisons using the non-parametric test statistic developed by Slotnick, Moo, Segal, and Hart (2003), which requires a cluster extent of 49 voxels for a corrected p < .05 (at a whole brain uncorrected threshold of p < .005). RESULTS A Unusual Intention > Normal contrast revealed significant activation only in the dorsal anterior
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AMPE ET AL. TABLE 1 Contrasts of Unusual Intention and Unusual Means against Normal action MNI coordinates Anatomical label Unusual Intention > Normal dorsal ACC Unusual Means > Normal L Postcentral Gyrus
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R Inferior Parietal Lobule (incl. aIPS)
L Superior Parietal Lobule (incl. aIPS) R Middle Occipital Gyrus R Inferior Temporal Gyrus (incl. EBA) R Inferior Temporal Gyrus L Middle Occipital Gyrus L Middle Temporal Gyrus (incl. EBA) Unusual Intention & Means > Normal
x
y
z
Voxels
Max t
−2 0
8 0
30 36
57
3.42 3.11
−44 −34 −46 34 34 34 −28 −32 34 52 44 −46 −46
−40 −38 −30 −44 −42 −40 −62 −60 −92 −72 −56 −68 −60
66 72 48 52 72 64 66 58 16 −8 −10 −2 6
463
5.18a 4.21 3.84 4.05a 3.92 3.77 3.78 3.29 5.88a 5.26 4.91 3.37a 4.20
488
53 1561
394
No suprathreshold clusters Coordinates in MNI (Montreal Neurological Institute) stereotactic space of local maxima within each cluster. The reported clusters survive a whole brain uncorrected threshold of p < .005 and are significant after correction for multiple comparisons according to the Slotnick test statistic (cluster size > 49). Regions denoted by a are also significant after FDR correction for multiple comparisons at cluster level (p < .05). Only subpeaks with a different anatomy are relabeled. ACC, Anterior Cingulate Cortex; EBA, Extrastriate Body Area; aIPS, anterior IntraParietal Sulcus; L, Left; R, Right; incl., including.
cingulate cortex – dACC; Table 1, Figure 1A). The Unusual Means > Normal contrast showed significant activation in the predicted areas, including the bilateral EBA embedded in the temporal cortex and the bilateral aIPS embedded in the parietal lobule. In addition, there was activation in the left postcentral gyrus and the bilateral middle occipital gyrus. The contrast combining both Intention and Means violations > Normal showed no effects. To explore whether the lack of activation in mentalizing areas in the Unusual Intention > Normal contrast was due to low sensitivity of the wholebrain analysis, we also conducted a region of interest (ROI) analysis with small volume correction of key mentalizing regions. We constructed ROIs with spheres of 8 mm around coordinates derived from the meta-analyses by Van Overwalle (2009) and Van Overwalle and Baetens (2009) for the bilateral TPJ (±50, –55, 25) and mPFC (0, 50, 20). These analyses revealed no significant effect (Figure 1B; all clusters had 0 voxels at p < .005 uncorrected). We also extracted the percentage signal change from the same ROIs with a 15 mm radius. There was no significant effect of condition in any ROI (all Fs < 1).
DISCUSSION Recent evidence suggests that observing an unusual action (intention) triggers the mentalizing network instead of, or in addition to, the mirror network. The aim of this study was to investigate whether mentalizing activation for unusual actions also occurs under minimal conditions that do not explicitly invite observers to infer the intention of an actor and do not draw attention away from the whole action (to avoid focusing on intentionirrelevant aspects of the action). To begin with our main hypothesis, we did not find mentalizing activity when people observed actions with an unusual intention (i.e., unusual object locations) under minimal viewing conditions. Surprisingly, we also failed to detect mirror activity in this condition, contrary to de Lange et al. (2008). Instead we found significant activation in the dACC. As this latter area is involved in conflict detection and monitoring (Botvinick, Cohen, & Carter, 2004), this suggests that participants noticed that there was a violation of the typical behavioral execution in this type of actions. With respect to unusual means (e.g., unusual hand grip), in line with de Lange et al. (2008),
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Figure 1. (A) Unusual Intention and Unusual Means. Whole brain view with uncorrected threshold of p < .005 and cluster volume > 49 voxels. Circles denote ROI. (B) Percent signal change for core mentalizing ROIs. dACC, dorsal Anterior Cingulate Cortex; mPFC, medial PreFrontal Cortex (ROI); SPL, Superior Parietal Lobule; aIPS, anterior IntraParietal Sulcus; TPJ, Temporo-Parietal Junction (ROI); MOG, Middle Occipital Gyrus; EBA, Extrastriate Body Area. [To view this figure in color, please visit the online version of this Journal.]
we found that observing actions performed with unusual means versus normal actions activated the EBA, an area associated with the visual processing of the human body (Downing, Jiang, Shuman, & Kanwisher, 2001; Peelen & Downing, 2007). We also observed activations in the right aIPS which is part of the mirror network (Rizzolatti & Craighero, 2004; Van Overwalle & Baetens, 2009) and in temporal and parietal areas that are part of a “functional circuit” involved in practical (and to some extent conceptual) tool-use knowledge (for a review, see Lewis, 2006). There might be several reasons why mentalizing activity for unusual actions was not observed under minimal instructions. One interesting explanation is the poor context in which the action was embedded which might have reduced the social
relevance to the observer and hence his or her spontaneous motivation to make mentalizing inferences. In our study, apart from the object held by the same person in front of the same white background, there were no contextual clues that could inform the observer about the meaning or the unusualness of the action. Most other relevant studies depicted unusual actions in a much richer context. For instance, in Brass et al. (2007), a light switch was operated with a knee (rather than finger) while the actor’s hands were empty (implausible action) versus while both hands were occupied by a stack of books (plausible action; see also Liepelt et al., 2008). Note that participants paid sufficient attention to the material itself in the present study, because most of them detected the inconsistency and showed activity in the relevant brain area (dACC).
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Another explanation is that perhaps participants could easily generate plausible alternative goals for the unusual actions. Our pilot study shows that, remarkably, the majority of participants had no difficulty in finding a goal for unusual actions (on average 77% gave a plausible goal; e.g., in the case where the person is holding a camera to her ear, participants came up with goals such as “listening to the camera to check whether it still works”). Under the scanner, this ease may have triggered little additional mentalizing (or even mirror) activity in comparison with normal actions. Perhaps, this ease of goal explanation might have been true also for actions with combined unusual intention and means (although we have no pilot data on this condition), which may explain why these elicited no activation compared to normal actions. Still another explanation for the lack of activation in mentalizing brain areas is the modification of de Lange et al.’s (2008) blocked design (blocks of 6–7 stimuli from the same condition) into the present event-related design using a randomized stimulus order. Although this event-related design might have reduced the statistical sensitivity for detecting mentalizing activity relative to a blocked design, a more focused analysis on key regions of interest failed to reveal even a single significant voxel. Nevertheless, decreased statistical power remains a viable explanation for the present null results, as well as reduced psychological sensitivity and interest to unusualness due to a random stimulus presentation, aggravated by the bare social context discussed earlier. In summary, unusual action intentions do not always trigger the mentalizing network. We interpret this null result as suggesting that when there are not enough contextual clues explaining the unusualness of an action, people only notice that there is something unusual about the action, but do not spontaneously mentalize about why the actor behaves strangely. In order to trigger the mentalizing network, either a richer action context or an explicit instruction to attend to the intention might be a prerequisite. Further research is necessary to explore the respective contributions of the mirror and mentalizing networks in understanding unusual behavior. Manuscript received 12 January 2012 Revised manuscript received 15 October 2012 First published online 27 November 2012
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