Edited by: Agustin Ibanez, Institute of Cognitive Neurology, Argentina
Reviewed by: Aldo Ragazzoni, University of Florence, Italy; Blas Couto, Institute of Cognitive Neurology, Argentina
*Correspondence: Stephanie Cacioppo, High-Performance Electrical NeuroImaging Laboratory, Department of Psychology, Center for Cognitive and Social Neuroscience, The University of Chicago, 5848 S. University Avenue, Chicago, IL 60637, USA. e-mail:
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
Although significant advances have been made in our understanding of the neural basis of action observation and intention understanding in the last few decades by studies demonstrating the involvement of a specific brain network (action observation network; AON), these have been largely based on experimental studies in which people have been considered as strictly isolated entities. However, we, as social species, spend much more of our time performing actions interacting with others. Research shows that a person's position along the continuum of perceived social isolation/bonding to others is associated with a variety of physical and mental health effects. Thus, there is a crucial need to better understand the neural basis of intention understanding performed in interpersonal and emotional contexts. To address this issue, we performed a meta-analysis using of functional magnetic resonance imaging (fMRI) studies over the past decade that examined brain and cortical network processing associated with understanding the intention of others actions vs. those associated with passionate love for others. Both overlapping and distinct cortical and subcortical regions were identified for intention and love, respectively. These findings provide scientists and clinicians with a set of brain regions that can be targeted for future neuroscientific studies on intention understanding, and help develop neurocognitive models of pair-bonding.
Throughout the past three decades, a growing number of studies have shown that one understands actions and intentions of other people by shaping one's understanding and anticipation of the environment based on one's own motor system (Jeannerod,
Although these findings provide valuable information about the brain mechanisms involved in the understanding of actions performed by strangers, they do not tell much about the brain mechanisms involved in the understanding of a significant other [a person with whom the participant intends to be with (i.e., a participant's partner in an intimate relationship or a best friend in an companionate relationship)]. To date, studies on intention understanding have been largely based on functional magnetic resonance imaging (fMRI) studies in which participants have been considered as strictly isolated entities i.e., focusing mostly on the action type rather than on the relationship with the agent and the observer. However, people typically spend most of their time in social settings interacting with significant others. Research shows that a person's position along the continuum of perceived social isolation/bonding to others is associated with a variety of physical and mental health effects (Cacioppo and Cacioppo,
As a consequence, there is a health-related need to better understand the functional dynamic of our brain during actions performed in an interpersonal context. This is critical as we spend much of our lifetime interacting with significant others, acquaintances, as well as strangers.
A growing body of research in psychology highlights the importance of studying the processing of significant others by demonstrating the influence of implicit processing of significant others (compared to strangers) on the individual's perception and cognitive processes. For instance, evidence suggests that the emotional bond between an actor and a perceiver may facilitate mutual intention perception, with a stronger bond associated with faster intention understanding (Cutting and Kozlowski,
Inspired by the theories on embodied cognition and simulation theories, one explanation for this facilitation effect is that intention understanding may be based, in part, upon mechanisms of self-expansion among significant others. Through self-expansion mechanisms, a collective unconscious mental representation may be formed among individuals who share self-characteristics, values, and actions in a common environment (Agnew and Etcheverry,
To test this hypothesis, we statistically explored the neural similarities and differences of the neural bases between intention and passionate love for a partner by performing a meta-analysis of fMRI studies involving intention understanding and love, respectively.
We performed a systematic review of functional neuroimaging studies of intention understanding and passionate love, respectively. All papers and books in the literature published up to May 2011 (inclusive) were considered for this review, subject to two general limitations: the publication had to be a manuscript, chapter or book, and the title and abstract had to be available in English. Materials were identified through computer-based search, as described below.
Our systematic computer-based search was based on the published literature of functional neuroimaging studies on intention understanding using MEDLINE library through PubMed database. Key words used for this search were “intention understanding,” “action understanding,” “fMRI,” and “neuroimaging.” Publications were selected on the basis of the following criteria: (1) fMRI neuroimaging studies; (2) with healthy adult participants, and (3) paradigms included stories (text or cartoons) or video-clips on intention understanding only. In all selected studies, participants' instruction was either to observe intentions, to infer the intentions of the actions performed by others, or to answer questions about the intention of the actions (i.e., “why”). In all the studies we classified as “intention understanding” agents were strangers (unfamiliar people) only. A list of the studies and contrast conditions for intention understanding are shown in Table
We similarly performed a computer-based search of functional neuroimaging studies on passionate love using MEDLINE library through PubMed database. Expanding on our earlier study (Ortigue et al.,
To provide readers with a synthesized and statistical view of the common and different brain networks mediating intention understanding and passionate love, we analyzed the distribution of peak coordinates related to intention understanding (Figure
Based on our search criteria, we found a total of 25 fMRI studies. This included 17 studies (21 experimental paradigms) for intention understanding (Table
Results confirm previous studies by demonstrating that understanding intentions of strangers involved the brain areas involved in both SN and AON, including areas sustaining embodied cognition, simulation, and self-other perception (such as vMPFC, BA6, MTG/STG, Angular gyrus, see Table
Our fMRI meta-analysis revealed a shared brain network between intention understanding and passionate love (Figure
The present research highlights a shared network between love and intention, which includes (1) areas that overlap with areas related to dopamine circuits; and (2) several regions implicated in social cognition, embodied cognition, attachment, mental state representation, and self-representation. These results are consistent with previous studies indicating that both love and intention involve goal-directed and rewarding behaviors towards a specific partner. The recruitment of dorsal parts of the striatum, such as the caudate and putamen, which are innervated by dopamine coming from both the VTA and substantia nigra, is in line with recent work in animals showing that these brain areas are critical in the development of a pair bond and conditioned partner preference (Pfaus,
The overlap between passionate love and intention understanding in brain areas, such as the vMPFC, is consistent with a growing body of studies unraveling the recruitment of this brain area during tasks that require introspections about self and by tasks that require inferences about the minds of others perceived to be similar to self (Jenkins et al.,
By identifying specific functional brain regions and networks in a large sample of healthy subjects, the present analysis reinforces the consistency and specificity of the brain regions that are being reported in the burgeoning body of studies on love and intention understanding. Interestingly, by revealing an additive brain network for both intention understanding and passionate love, the present findings offer a new way to look at the neurobiology of the loving mind during embodied cognition through the lens of a specific subset of AON and SN regions of interest. This provides scientists and clinicians with a unique and strong rationale to further investigate neurocognitive models that may explain the modulations of these common regions and brain networks in future studies on intention understanding in dyads.
One limitation of the present meta-analysis study was some of the fMRI studies of intention contrasted the condition of interest either to resting state(s) (e.g., Iacoboni et al.,
The authors disclosed receipt of the following financial support for the research and/or authorship of this article: Swiss National Science Foundation (Grant #PP00_1_128599/1 to Stephanie Cacioppo), the Mind Science Foundation (Grant #TSA2010-2 to Stephanie Cacioppo, Francesco Bianchi-Demicheli), NCRR NIH COBRE Grant E15524 (Grant #E15524 to the Sensory Neuroscience Research Center of West Virginia University to James W. Lewis), the MOE Project of Key Research Institute of Humanities and Social Sciences (Grant #12JJD190004 to Yi-Wen Wang), and the Program for New Century Excellent Talents in Universities (Grant #NCET-11-1065 to Yi-Wen Wang).
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Brass | 2007 | 15 | 7 | 15 | Video-clips | Implausible > ordinary motion |
Buccino | 2007 | 20 | 10 | 20 | Video-clips | Attend to intention > viewing |
Video-clips | Incorrect unintended motion > ordinary motion | |||||
Carter | 2011 | 17 | 8 | 15 | Video-clips | Human reaching movements: goal shift > goal miss |
Ciaramidaro | 2007 | 12 | 6 | 12 | Comic strips | Intentional (communicative) > physical event |
Comic strips | Intentional (social) > physical event | |||||
Comic strips | Intentional (private) > physical event | |||||
de Lange | 2008 | 19 | 10 | 19 | Pictures | Ordinary > extraordinary intentions |
den Ouden | 2005 | 11 | 11 | Not specified | Scenarios | Intentional action > physical event |
Hamilton | 2006 | 20 | 11 | 19 | Video-clips | Repetition suppression for action goal |
Hamilton | 2008 | 20 | 13 | 20 | Video-clips | Repetition suppression for action outcome |
Iacoboni | 2005 | 23 | 15 | 23 | Video-clips | Hand grasping > rest |
Jastorff | 2011 | 15 | 9 | 15 | Video-clips | Non-rational > rational movements |
Liew | 2010 | 18 | 8 | 18 | Video-clips | Hand gestures > still control |
Newman-Norlund | 2010 | 18 | 10 | 18 | Video-clips | Object-directed actions > rest |
Ortigue | 2009 | 24 | 0 | 24 | Video-clips | Repetition suppression for intention |
Pelphrey | 2004 | 12 | 7 | 12 | Video-clips | Incorrect > correct motion |
Ramsey | 2010 | 25 | 17 | 24 | Video-clips | Repetition suppression for object-goal |
Walter (1) | 2004 | 13 | 7 | 13 | Comic strips | Intentional action > physical event |
Walter (2) | 2004 | 12 | 6 | 12 | Comic strips | Intentional action > physical event |
Wang | 2006 | 12 | 6 | 12 | Scenarios | Attend to face > rest |
Total | 306 | 161 | 291 |
Acevedo | 2012 | 17 | 10 | 17 | Faces | Partner > high familiar acquaintance |
Faces | Partner > close friend | |||||
Aron | 2005 | 17 | 10 | 17 | Faces | Beloved > familiar neutral acquaintance |
Bartels | 2000 | 17 | 11 | 16 | Faces | Beloved > friend |
Kim | 2009 | 10 | 5 | 10 | Faces | Beloved > friend (early) |
Faces | Beloved > friend (late) | |||||
Ortigue | 2007 | 36 | 36 | 36 | Names | Beloved > friend or stranger |
Stoessel | 2011 | 12 | 6 | 12 | Pictures | Beloved > erotic (happy condition) |
Xu | 2011 | 18 | 10 | 18 | Faces | Beloved > familiar neutral acquaintance |
Zeki | 2010 | 24 | Not specified | Not specified | Faces | Beloved > neutral |
Total | 151 | 88 | 126 |
vmPFC | 6 | 52 | −12 | 4000 | ||||
Inferior frontal gyrus (p. Opercularis) (BA 44: 20%) | 46 | 10 | 27 | 17904 | ||||
Superior frontal gyrus (BA 6: 50%) | −18 | 2 | 67 | 7048 | ||||
SMA (BA 6: 20%) | −6 | 20 | 51 | 6648 | ||||
BA 6 (20%) | 20 | −5 | 48 | 40 | ||||
Precentral gyrus (BA 6: 60%) | 36 | −12 | 58 | 4120 | ||||
Precentral gyrus (BA 44: 30%) | −46 | 7 | 33 | 29,424 | ||||
BA 45 (10%) | 37 | 33 | 0 | 3184 | ||||
Middle temporal gyrus/STG | −47 | −50 | 18 | 73,992 | ||||
Heschls gyrus (Insula/Ig1: 60%; TE1.1: 50%; OP2: 30%) | −33 | −28 | 13 | 464 | ||||
Gyrus ambiens | 46 | −6 | −23 | 7688 | ||||
Angular gyrus (IPC/PFm: 20%; PGa: 20%; hIP1: 10%) | 47 | −46 | 24 | 73,608 | ||||
Precuneus (SPL/7P: 20%; SPL/7A: 20%) | −2 | −55 | 47 | 17,744 | ||||
Anterior cingulate cortex | −3 | 49 | 11 | 10,424 | ||||
7 | 41 | 29 | 7928 | |||||
Middle cingulate cortex (BA 6: 10%) | 10 | −6 | 44 | 2864 | ||||
Posterior cingulate cortex | 12 | −41 | 10 | 7736 | ||||
Putamen | −26 | 10 | −6 | 4120 | ||||
Fornix | −4 | −2 | 10 | 4120 | ||||
Calcarine gyrus (BA 17: 50%; BA 18: 10%) | 16 | −82 | 14 | 4088 | ||||
Calcarine gyrus (BA 17: 70%; BA 18: 20%) | 23 | −99 | −2 | 3424 | ||||
Middle occipital gyrus (IPC/PGp: 30%) | −35 | −84 | 29 | 3024 | ||||
Optic radiations | −26 | −34 | 10 | 2336 |
vmPFC | 10 | 39 | −11 | 2744 | ||||
−5 | 49 | −8 | 9384 | |||||
dlPFC | −7 | 51 | 22 | 5056 | ||||
SMA (BA 6: 60%; BA 4: 10%) | 10 | −18 | 61 | 24,760 | ||||
Postcentral gyrus (BA 3b: 60%; BA 1: 10%; BA 6: 10%) | 61 | −3 | 24 | 6784 | ||||
Superior temporal gyrus (TE3: 10%) | 63 | −14 | −6 | 3656 | ||||
Superior temporal gyrus (IPC/PFcm: 10%; OP1: 10%; TE1.1: 10%) | −56 | −28 | 8 | 4120 | ||||
Posterior middle temporal gyrus (V5: 10%) | −55 | −67 | 2 | 3312 | ||||
Inferior temporal gyrus | −40 | −8 | −28 | 4120 | ||||
Middle cingulate cortex | 10 | 5 | 32 | 16 | ||||
Supramarginal gyrus (IPC/PFm: 70%; IPC/PF: 30%; IPC/PGa: 20%) | 62 | −45 | 25 | 7040 | ||||
Supramarginal gyrus (IPC/PF: 60%; IPC/PFm: 40%; IPC/PFcm: 10%) | −63 | −46 | 25 | 4096 | ||||
Superior parietal lobule (SPL/7A: 40%; BA2: 30%; SPL/5L: 30%) | −23 | −50 | 53 | 3128 | ||||
PGa (10%) | 40 | −48 | 15 | 16 | ||||
Calcarine gyrus (BA 17: 100%; BA 18: 30%) | 9 | −90 | 1 | 22,440 | ||||
Cuneus | 18 | −70 | 24 | 6192 | ||||
Thalamus | −3 | −12 | 1 | 284,552 | ||||
Cerebellum | 42 | −57 | −28 | 7512 | ||||
34 | −45 | −48 | 6656 | |||||
−36 | −78 | −40 | 3896 | |||||
Superior frontal gyrus | −24 | 12 | 66 | 648 | ||||
Posterior superior temporal gyrus (IPC: 50%) | −50 | −38 | 18 | 600 | ||||
Superior medial frontal gyrus | −9 | 27 | 59 | 1288 | ||||
−10 | 52 | 16 | 632 | |||||
Middle orbital gyrus/orbitofrontal | 2 | 62 | −8 | 648 | ||||
Gyrus rectus (orbitofrontal) | −4 | 60 | −24 | 648 | ||||
Middle frontal gyrus | −30 | 54 | 2 | 648 | ||||
Superior anterior medial frontal gyrus | 8 | 54 | 22 | 1272 | ||||
11 | 65 | 5 | 1264 | |||||
Inferior frontal gyrus (p. orbitalis) | 35 | 33 | −8 | 1200 | ||||
Inferior frontal gyrus (p. triangularis) | −37 | 28 | 0 | 16 | ||||
−37 | 26 | −2 | 16 | |||||
−33 | 35 | −2 | 824 | |||||
56 | 28 | 8 | 648 | |||||
Middle frontal gyrus | 30 | 47 | 4 | 1200 | ||||
−30 | 44 | 11 | 344 | |||||
Anterior cingulate cortex | 8 | 40 | 9 | 1152 | ||||
8 | 28 | 16 | 648 | |||||
−6 | 42 | −6 | 600 | |||||
Middle cingulate cortex | 4 | −22 | 42 | 648 | ||||
12 | −22 | 34 | 616 | |||||
14 | −20 | 43 | 40 | |||||
Posterior cingulate cortex | −1 | −32 | 26 | 2440 | ||||
Inferior temporal gyrus/fusiform area | 42 | −52 | −12 | 648 | ||||
Superior temporal gyrus | −50 | −28 | 2 | 648 | ||||
Temporal pole | 40 | 8 | −28 | 648 | ||||
−34 | 18 | −22 | 648 | |||||
Caudate nucleus | 54 | −32 | 8 | 648 | ||||
−8 | 20 | 0 | 648 | |||||
17 | 1 | 23 | 1024 | |||||
10 | 16 | 5 | 1136 | |||||
Insula | 39 | −6 | −7 | 2632 | ||||
−42 | −9 | −6 | 2112 | |||||
−36 | 18 | −4 | 648 | |||||
−34 | −22 | 10 | 608 | |||||
SMA | −1 | 10 | 65 | 1296 | ||||
4 | 4 | 52 | 648 | |||||
Thalamus | −8 | −9 | −2 | 1288 | ||||
10 | −24 | 10 | 648 | |||||
Heschel gyrus | 45 | −17 | 8 | 1280 | ||||
Cerebellum | 10 | −44 | −7 | 1168 | ||||
Cerebellar vermis | −2 | −58 | −10 | 648 | ||||
Putamen | −22 | 7 | −8 | 1024 | ||||
−18 | 19 | −9 | 896 | |||||
Precuneus | 8 | −51 | 22 | 976 | ||||
Parahippocampal region (Amygdala: 10%) | 19 | 2 | −13 | 896 | ||||
Pallidum | 22 | −1 | 6 | 888 | ||||
Rolandic operculum | 60 | −14 | 12 | 648 | ||||
Postcentral gyrus | −62 | −4 | 22 | 600 | ||||
Lingual gyrus (Hippocampus: 40%) | −11 | −38 | −10 | 424 |
dlPFC | 2 | 41 | 36 | 32 | ||||
−5 | 54 | 19 | 2000 | |||||
vmPFC | 9 | 45 | −11 | 280 | ||||
4 | 55 | −11 | 1904 | |||||
Superior frontal gyrus (BA 6: 40%) | 30 | −12 | 62 | 424 | ||||
Inferior frontal gyrus (p. Orbitalis) | 39 | 31 | −4 | 824 | ||||
Inferior frontal gyrus (p. Triangularis) (BA 45: 60%) | 50 | 30 | 16 | 632 | ||||
Inferior frontal gyrus (p. Triangularis) (BA 45: 60%; BA 44: 20%) | −46 | 24 | 21 | 5232 | ||||
Inferior frontal gyrus (p. Opercularis) | 39 | 18 | 13 | 232 | ||||
Inferior frontal gyrus (p. Opercularis) (BA 44: 40%) | 56 | 9 | 21 | 272 | ||||
Postcentral gyrus (IPC/PFop: 30%; OP4: 30%; OP3: 10%) | 62 | −16 | 23 | 1248 | ||||
Postcentral gyrus (BA 2: 80%; SPL/7PC: 20%; BA 3b: 10%) | 28 | −42 | 57 | 1104 | ||||
SMA (BA 6: 70%) | 4 | −5 | 48 | 48 | ||||
SMA | −6 | 21 | 47 | 2024 | ||||
SMA (BA 6: 60%) | −10 | −5 | 69 | 80 | ||||
Inferior temporal gyrus | −49 | −51 | −20 | 3032 | ||||
Middle temporal gyrus (V5: 10%) | −53 | −68 | 2 | 2312 | ||||
Superior temporal gyrus (OP1: 10%) | −56 | −30 | 6 | 2424 | ||||
Superior temporal gyrus (IPC/PF: 60%; IPC/PFm: 30%; PGa: 20%) | −60 | −46 | 23 | 1648 | ||||
Supra marginal gyrus (IPC/PFm: 70%; IPC/PF: 30%; IPC/PGa: 30%) | 61 | −45 | 24 | 5800 | ||||
Anterior cingulate cortex | −7 | 40 | −2 | 744 | ||||
−7 | 30 | 6 | 224 | |||||
6 | 34 | 22 | 3696 | |||||
Posterior cingulate cortex | 7 | −40 | 14 | 3024 | ||||
−2 | −53 | 29 | 1088 | |||||
Superior parietal lobule (SPL/7PC: 30%; SPL/7A: 20%; hIP3: 10%) | −26 | −53 | 53 | 1096 | ||||
Lingual gyrus (BA 17: 50%; BA 18: 10%) | 29 | −59 | 3 | 904 | ||||
Inferior temporal gyrus | 46 | −56 | −23 | 776 | ||||
Cuneus (BA 18: 10%; BA 17: 10%) | 16 | −77 | 18 | 672 | ||||
Precuneus | 25 | −45 | 8 | 568 | ||||
Precuneus (SPL/5L: 40%; SPL/7a: 20%; SPL/5M: 10%) | −14 | −50 | 57 | 16 | ||||
Anterior insula (Id1: 40%) | 43 | −4 | −14 | 272 | ||||
Anterior insula | 35 | 28 | 5 | 256 | ||||
Hippocampus | 37 | −14 | −19 | 1224 | ||||
Putamen | −27 | 10 | −6 | 3488 | ||||
Fornix | −3 | −3 | 11 | 3368 | ||||
Calcarine gyrus (BA 17: 50%; BA 18: 10%) | 14 | −87 | 14 | 1424 | ||||
Calcarine gyrus (BA 17: 80%; BA 18: 10%) | 21 | −95 | −2 | 896 | ||||
Optic radiations | −26 | −36 | 11 | 1608 | ||||
−33 | −54 | −2 | 56 |