Brain Structure and Function

, Volume 218, Issue 5, pp 1211–1227

The “vegetarian brain”: chatting with monkeys and pigs?

  • Massimo Filippi
  • Gianna Riccitelli
  • Alessandro Meani
  • Andrea Falini
  • Giancarlo Comi
  • Maria A. Rocca
Original Article

Abstract

An array of brain regions in the fronto-parietal and temporal lobes cooperates to process observation and execution of actions performed by other individuals. Using functional MRI, we hypothesized that vegetarians and vegans might show brain responses to mouth actions performed by humans, monkeys, and pigs different from omnivores. We scanned 20 omnivores, 19 vegetarians, and 21 vegans while watching a series of silent videos, which presented a single mouth action performed by a human, a monkey, and a pig. Compared to omnivores, vegetarians and vegans have increased functional connectivity between regions of the fronto-parietal and temporal lobes versus the cerebellum during observation of mouth actions performed by humans and, to the same degree, animals. Vegans also had increased connectivity with the supplementary motor area. During human mouth actions, increased amygdala activity in vegetarians and vegans was found. More critically, vegetarians recruited the right middle frontal gyrus and insula, which are involved in social mirroring, whereas vegans activated the left inferior frontal gyrus and middle temporal gyrus, which are part of the mirror neuron system. Monkey mouth actions triggered language network activity in both groups, which might be due to the attempt to decode monkey mouth gesture, with an additional recruitment of associative temporo-occipital areas in vegans, whereas pig mouth actions activated empathy-related regions, including the anterior cingulum. These results support the role of the action observation–execution matching system in social cognition, which enables us to interact not only with our conspecifics but also with species in phylogenetic proximity to humans.

Keywords

Action observation–execution matching system Animals Humans Mouth action Vegetarians 

References

  1. Allison T, Puce A, McCarthy G (2000) Social perception from visual cues: role of the STS region. Trends Cogn Sci 4:267–278PubMedCrossRefGoogle Scholar
  2. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541PubMedCrossRefGoogle Scholar
  3. Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13:400–404PubMedGoogle Scholar
  4. Buccino G, Lui F, Canessa N, Patteri I, Lagravinese G, Benuzzi F, Porro CA, Rizzolatti G (2004) Neural circuits involved in the recognition of actions performed by nonconspecifics: an FMRI study. J Cogn Neurosci 16:114–126PubMedCrossRefGoogle Scholar
  5. Cauda F, Costa T, Torta DM, Sacco K, D’Agata F, Duca S, Geminiani G, Fox PT, Vercelli A (2012) Meta-analytic clustering of the insular cortex: characterizing the meta-analytic connectivity of the insula when involved in active tasks. Neuroimage 62:343–355PubMedCrossRefGoogle Scholar
  6. Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2012) Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb CortexGoogle Scholar
  7. Cheng Y, Lin CP, Liu HL, Hsu YY, Lim KE, Hung D, Decety J (2007) Expertise modulates the perception of pain in others. Curr Biol 17:1708–1713PubMedCrossRefGoogle Scholar
  8. Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118(Pt 1):279–306PubMedCrossRefGoogle Scholar
  9. Filippi M, Riccitelli G, Falini A, Di Salle F, Vuilleumier P, Comi G, Rocca MA (2010) The brain functional networks associated to human and animal suffering differ among omnivores, vegetarians and vegans. PLoS ONE 5:e10847PubMedCrossRefGoogle Scholar
  10. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678PubMedCrossRefGoogle Scholar
  11. Friston KJ, Holmes AP, Poline JB, Grasby PJ, Williams SC, Frackowiak RS, Turner R (1995) Analysis of fMRI time-series revisited. Neuroimage 2:45–53PubMedCrossRefGoogle Scholar
  12. Friston KJ, Holmes AP, Price CJ, Buchel C, Worsley KJ (1999) Multisubject fMRI studies and conjunction analyses. Neuroimage 10:385–396PubMedCrossRefGoogle Scholar
  13. Friston KJ, Penny WD, Glaser DE (2005) Conjunction revisited. Neuroimage 25:661–667PubMedCrossRefGoogle Scholar
  14. Gazzola V, Keysers C (2009) The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cereb Cortex 19:1239–1255PubMedCrossRefGoogle Scholar
  15. Grasby PM, Frith CD, Friston KJ, Bench C, Frackowiak RS, Dolan RJ (1993) Functional mapping of brain areas implicated in auditory–verbal memory function. Brain 116(Pt 1):1–20PubMedCrossRefGoogle Scholar
  16. Hein G, Knight RT (2008) Superior temporal sulcus—It’s my area: or is it? J Cogn Neurosci 20:2125–2136PubMedCrossRefGoogle Scholar
  17. Iacoboni M (2009) Imitation, empathy, and mirror neurons. Annu Rev Psychol 60:653–670PubMedCrossRefGoogle Scholar
  18. Jirak D, Menz MM, Buccino G, Borghi AM, Binkofski F (2010) Grasping language—a short story on embodiment. Conscious Cogn 19:711–720PubMedCrossRefGoogle Scholar
  19. Just MA, Carpenter PA, Keller TA, Eddy WF, Thulborn KR (1996) Brain activation modulated by sentence comprehension. Science 274:114–116PubMedCrossRefGoogle Scholar
  20. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120–131PubMedCrossRefGoogle Scholar
  21. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239PubMedCrossRefGoogle Scholar
  22. Murty VP, Ritchey M, Adcock RA, LaBar KS (2010) fMRI studies of successful emotional memory encoding: a quantitative meta-analysis. Neuropsychologia 48:3459–3469PubMedCrossRefGoogle Scholar
  23. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  24. Paulesu E, Perani D, Blasi V, Silani G, Borghese NA, De Giovanni U, Sensolo S, Fazio F (2003) A functional-anatomical model for lipreading. J Neurophysiol 90:2005–2013PubMedCrossRefGoogle Scholar
  25. Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16:331–348PubMedCrossRefGoogle Scholar
  26. Regan T (1985) The case for animal rights. University of California, Berkeley 422Google Scholar
  27. Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661–670PubMedCrossRefGoogle Scholar
  28. Shamay-Tsoory SG (2011) The neural bases for empathy. Neuroscientist 17:18–24Google Scholar
  29. Shamay-Tsoory SG, Aharon-Peretz J, Perry D (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132:617–627PubMedCrossRefGoogle Scholar
  30. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303:1157–1162PubMedCrossRefGoogle Scholar
  31. Singer T, Seymour B, O’Doherty JP, Stephan KE, Dolan RJ, Frith CD (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature 439:466–469PubMedCrossRefGoogle Scholar
  32. Tettamanti M, Buccino G, Saccuman MC, Gallese V, Danna M, Scifo P, Fazio F, Rizzolatti G, Cappa SF, Perani D (2005) Listening to action-related sentences activates fronto-parietal motor circuits. J Cogn Neurosci 17:273–281PubMedCrossRefGoogle Scholar
  33. Thompson KL, Gullone E (2003) Promotion of empathy and prosocial behaviour in children through humane education. Australian Psychologist 38:175–182Google Scholar
  34. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289PubMedCrossRefGoogle Scholar
  35. Xiang HD, Fonteijn HM, Norris DG, Hagoort P (2010) Topographical functional connectivity pattern in the perisylvian language networks. Cereb Cortex 20:549–560PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Massimo Filippi
    • 1
    • 2
  • Gianna Riccitelli
    • 1
  • Alessandro Meani
    • 1
  • Andrea Falini
    • 3
  • Giancarlo Comi
    • 2
  • Maria A. Rocca
    • 1
    • 2
  1. 1.Neuroimaging Research Unit, Institute of Experimental Neurology, Division of NeuroscienceSan Raffaele Scientific Institute, “Vita-Salute” San Raffaele UniversityMilanItaly
  2. 2.Department of NeurologySan Raffaele Scientific Institute, “Vita-Salute” San Raffaele UniversityMilanItaly
  3. 3.Department of NeuroradiologySan Raffaele Scientific Institute, “Vita-Salute” San Raffaele UniversityMilanItaly

Personalised recommendations