Human, Nature, Dynamism: The Effects of Content and Movement Perception on Brain Activations during the Aesthetic Judgment of Representational Paintings

Movement perception and its role in aesthetic experience have been often studied, within empirical aesthetics, in relation to the human body. No such specificity has been defined in neuroimaging studies with respect to contents lacking a human form. The aim of this work was to explore, through functional magnetic imaging (f MRI), how perceived movement is processed during the aesthetic judgment of paintings using two types of content: human subjects and scenes of nature. Participants, untutored in the arts, were shown the stimuli and asked to make aesthetic judgments. Additionally, they were instructed to observe the paintings and to rate their perceived movement in separate blocks. Observation highlighted spontaneous processes associated with aesthetic experience, whereas movement judgment outlined activations specifically related to movement processing. The ratings recorded during aesthetic judgment revealed that nature scenes received higher scored than human content paintings. The imaging data showed similar activation, relative to baseline, for all stimuli in the three tasks, including activation of occipito-temporal areas, posterior parietal, and premotor cortices. Contrast analyses within aesthetic judgment task showed that human content activated, relative to nature, precuneus, fusiform gyrus, and posterior temporal areas, whose activation was prominent for dynamic human paintings. In contrast, nature scenes activated, relative to human stimuli, occipital and posterior parietal cortex/precuneus, involved in visuospatial exploration and pragmatic coding of movement, as well as central insula. Static nature paintings further activated, relative to dynamic nature stimuli, central and posterior insula. Besides insular activation, which was specific for aesthetic judgment, we found a large overlap in the activation pattern characterizing each stimulus dimension (content and dynamism) across observation, aesthetic judgment, and movement judgment tasks. These findings support the idea that the aesthetic evaluation of artworks depicting both human subjects and nature scenes involves a motor component, and that the associated neural processes occur quite spontaneously in the viewer. Furthermore, considering the functional roles of posterior and central insula, we suggest that nature paintings may evoke aesthetic processes requiring an additional proprioceptive and sensori-motor component implemented by “motor accessibility” to the represented scenario, which is needed to judge the aesthetic value of the observed painting.

[1]  Scott L. Fairhall,et al.  Neural correlates of object indeterminacy in art compositions , 2008, Consciousness and Cognition.

[2]  A. Jacobs Cognitive Neuroscience of Natural Language Use: Towards a neurocognitive poetics model of literary reading , 2014 .

[3]  Helmut Leder,et al.  Art in Time and Space: Context Modulates the Relation between Art Experience and Viewing Time , 2014, PloS one.

[4]  C. Gross Single neuron studies of inferior temporal cortex , 2008, Neuropsychologia.

[5]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[6]  V. Gallese,et al.  How Stories Make Us Feel: Toward an Embodied Narratology , 2011 .

[7]  Giacomo Rizzolatti,et al.  The neural correlates of 'vitality form' recognition: an fMRI study: this work is dedicated to Daniel Stern, whose immeasurable contribution to science has inspired our research. , 2014, Social cognitive and affective neuroscience.

[8]  E. W. Lauer,et al.  Somatovisceral motor patterns in the insula , 1961, The Journal of comparative neurology.

[9]  Oshin Vartanian,et al.  Neuroanatomical correlates of aesthetic preference for paintings , 2004, Neuroreport.

[10]  G. Luppino,et al.  Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5 , 2011, Brain Structure and Function.

[11]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[12]  J. Wessberg,et al.  Coding of pleasant touch by unmyelinated afferents in humans , 2009, Nature Neuroscience.

[13]  T. Kochiyama,et al.  Difference in brain activations during appreciating paintings and photographic analogs , 2014, Front. Hum. Neurosci..

[14]  H Burton,et al.  Somatotopographic organization in the second somatosensory area of M. fascicularis , 1980, The Journal of comparative neurology.

[15]  G. Rizzolatti,et al.  Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. , 2014, Physiological reviews.

[16]  M. E. Lewis,et al.  Opiate receptor gradients in monkey cerebral cortex: correspondence with sensory processing hierarchies. , 1981, Science.

[17]  Marina Weber,et al.  Elements Of Episodic Memory , 2016 .

[18]  V. Gallese,et al.  Exploring Responses to Art in Adolescence: A Behavioral and Eye-Tracking Study , 2014, PloS one.

[19]  C D Frith,et al.  Brain activity during memory retrieval. The influence of imagery and semantic cueing. , 1996, Brain : a journal of neurology.

[20]  D. Yves von Cramon,et al.  Brain correlates of aesthetic judgment of beauty , 2006, NeuroImage.

[21]  A. Jacobs,et al.  Fiction feelings in Harry Potter: haemodynamic response in the mid-cingulate cortex correlates with immersive reading experience , 2014, Neuroreport.

[22]  Preston P. Thakral,et al.  A neural mechanism for aesthetic experience , 2012, Neuroreport.

[23]  R. Kaplan,et al.  The Experience of Nature: A Psychological Perspective , 1989 .

[24]  H. Leder,et al.  A model of aesthetic appreciation and aesthetic judgments. , 2004, British journal of psychology.

[25]  Enrico Giora,et al.  How do painters represent motion in garments? Graphic invariants across centuries. , 2008, Spatial vision.

[26]  Howard Wainer,et al.  The Most Dangerous Equation , 2021, Picturing the Uncertain World.

[27]  A. Jacobs,et al.  Immersing in the stillness of an early morning: Testing the mood empathy hypothesis of poetry reception. , 2014 .

[28]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[29]  Sylvain Rheims,et al.  Functional connectivity of insular efferences , 2014, Human brain mapping.

[30]  A. Jacobs Neurocognitive poetics: methods and models for investigating the neuronal and cognitive-affective bases of literature reception , 2015, Front. Hum. Neurosci..

[31]  D. Stern The interpersonal world of infant , 1985 .

[32]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  H. Müller-Gärtner,et al.  Encoding and retrieval in declarative learning: a positron emission tomography study , 1998, Behavioural Brain Research.

[34]  O. Vartanian,et al.  Neural correlates of viewing paintings: Evidence from a quantitative meta-analysis of functional magnetic resonance imaging data , 2014, Brain and Cognition.

[35]  J. Decety,et al.  Top down effect of strategy on the perception of human biological motion: a pet investigation. , 1998, Cognitive neuropsychology.

[36]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[37]  S. M. Williams,et al.  The Premotor Cortex , 2001 .

[38]  Vittorio Gallese,et al.  Differential Involvement of Somatosensory and Interoceptive Cortices during the Observation of Affective Touch , 2011, Journal of Cognitive Neuroscience.

[39]  Thomas H. Leahey,et al.  Emerging Visions of the Aesthetic Process: Psychology, Semiology, and Philosophy. , 1994 .

[40]  G. Rizzolatti,et al.  The mirror mechanism: recent findings and perspectives , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  D. Wolpert,et al.  Maintaining internal representations: the role of the human superior parietal lobe , 1998, Nature Neuroscience.

[42]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[43]  David P. Friedman,et al.  Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch , 1986, The Journal of comparative neurology.

[44]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

[45]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[46]  Z. Cattaneo,et al.  A TMS study on the contribution of visual area V5 to the perception of implied motion in art and its appreciation , 2017, Cognitive neuroscience.

[47]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[48]  Ulrich Kirk,et al.  The Neural Basis of Object-Context Relationships on Aesthetic Judgment , 2008, PloS one.

[49]  Katrin Amunts,et al.  Cytoarchitecture and probabilistic maps of the human posterior insular cortex. , 2010, Cerebral cortex.

[50]  Giacomo Rizzolatti,et al.  Expressing our internal states and understanding those of others , 2015, Proceedings of the National Academy of Sciences.

[51]  Yizhou Wang,et al.  Matching Reality in the Arts: Self-Referential Neural Processing of Naturalistic Compared to Surrealistic Images , 2012, Perception.

[52]  Thomas Jacobsen,et al.  Electrophysiological indices of processing aesthetics: Spontaneous or intentional processes? , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[53]  G. Orban,et al.  The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors , 2010, The Journal of Neuroscience.

[54]  Russell A. Epstein,et al.  Common and Unique Representations in pFC for Face and Place Attractiveness , 2015, Journal of Cognitive Neuroscience.

[55]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[56]  N. Schwarz,et al.  Processing Fluency and Aesthetic Pleasure: Is Beauty in the Perceiver's Processing Experience? , 2004, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[57]  D. Berlyne,et al.  Aesthetics and Psychobiology , 1975 .

[58]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

[59]  Rebecca F. Schwarzlose,et al.  Separate face and body selectivity on the fusiform gyrus. , 2010, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  Johan Wessberg,et al.  Somatotopic Organization of Gentle Touch Processing in the Posterior Insular Cortex , 2009, The Journal of Neuroscience.

[61]  C. Saper The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. , 2002, Annual review of neuroscience.

[62]  Sylvain Rheims,et al.  Intrainsular functional connectivity in human , 2014, Human brain mapping.

[63]  M. Corbetta,et al.  Extrastriate body area in human occipital cortex responds to the performance of motor actions , 2004, Nature Neuroscience.

[64]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[65]  Marcos Nadal,et al.  The experience of art: insights from neuroimaging. , 2013, Progress in brain research.

[66]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[67]  N. Hadjikhani,et al.  Seeing Fearful Body Expressions Activates the Fusiform Cortex and Amygdala , 2003, Current Biology.

[68]  C. Mirasso,et al.  Sex-related similarities and differences in the neural correlates of beauty , 2009, Proceedings of the National Academy of Sciences.

[69]  Benny B. Briesemeister,et al.  10 years of BAWLing into affective and aesthetic processes in reading: what are the echoes? , 2015, Front. Psychol..

[70]  Mustafa Kamal Mohd Shariff,et al.  Landscape preference and human well-being , 2006 .

[71]  J. Mattingley,et al.  Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies , 2012, Neuroscience & Biobehavioral Reviews.

[72]  N. Kanwisher,et al.  Does the human brain process objects of expertise like faces? A review of the evidence , 2005 .

[73]  M. Trimble,et al.  The insular Lobe of Reil–its Anatamico-Functional, behavioural and Neuropsychiatric attributes in humans–a review , 2004, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[74]  Rudolf Stark,et al.  Parietal and premotor cortices: Activation reflects imitation accuracy during observation, delayed imitation and concurrent imitation , 2014, NeuroImage.

[75]  R. Arnheim To the Rescue of Art: Twenty-Six Essays , 1991 .

[76]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[78]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[79]  W. B. Pillsbury Attention in memory. , 2022 .

[80]  A. Murata,et al.  Cortical connections of the macaque anterior intraparietal (AIP) area. , 2008, Cerebral cortex.

[81]  Kevin A. Pelphrey,et al.  Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception , 2004, Journal of Cognitive Neuroscience.

[82]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[83]  F. Mauguière,et al.  Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. , 2002, Cerebral cortex.

[84]  W. Penfield,et al.  The insula; further observations on its function. , 1955, Brain : a journal of neurology.

[85]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[86]  M. Burke Literary Reading, Cognition and Emotion: An Exploration of the Oceanic Mind , 2010 .

[87]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[88]  Uta Boehm Humanscape Environments For People , 2016 .

[89]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[90]  D. Freedberg,et al.  Corticomotor Excitability during Observation and Imagination of a Work of Art , 2011, Front. Hum. Neurosci..

[91]  G. Rizzolatti,et al.  The Golden Beauty: Brain Response to Classical and Renaissance Sculptures , 2007, PloS one.

[92]  Stephan Wensveen,et al.  Aesthetic Interaction: A Framework , 2010, Design Issues.

[93]  David P. Friedman,et al.  A modality-specific somatosensory area within the insula of the rhesus monkey , 1993, Brain Research.

[94]  Aina Puce,et al.  Configural Processing of Biological Motion in Human Superior Temporal Sulcus , 2005, The Journal of Neuroscience.

[95]  V. Gallese,et al.  When Art Moves the Eyes: A Behavioral and Eye-Tracking Study , 2012, PloS one.

[96]  Roland Peyron,et al.  Role of Operculoinsular Cortices in Human Pain Processing: Converging Evidence from PET, fMRI, Dipole Modeling, and Intracerebral Recordings of Evoked Potentials , 2002, NeuroImage.

[97]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[98]  Mortimer Mishkin,et al.  Analogous neural models for tactual and visual learning , 1979, Neuropsychologia.

[99]  Daniel N. Stern,et al.  Forms of Vitality: Exploring Dynamic Experience in Psychology, the Arts, Psychotherapy, and Development , 2010 .

[100]  A. Jacobs,et al.  The quartet theory of human emotions: An integrative and neurofunctional model. , 2015, Physics of life reviews.

[101]  Vittorio Gallese,et al.  Emotional and Social Behaviors Elicited by Electrical Stimulation of the Insula in the Macaque Monkey , 2011, Current Biology.

[102]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[103]  P. Locher,et al.  Art on the plate: Effect of balance and color on attractiveness of, willingness to try and liking for food , 2010 .

[104]  N. Kanwisher,et al.  Activation in Human MT/MST by Static Images with Implied Motion , 2000, Journal of Cognitive Neuroscience.

[105]  Stefan Koelsch,et al.  Reading a Suspenseful Literary Text Activates Brain Areas Related to Social Cognition and Predictive Inference , 2015, PloS one.

[106]  H. Leder,et al.  Ten years of a model of aesthetic appreciation and aesthetic judgments : The aesthetic episode - Developments and challenges in empirical aesthetics. , 2014, British journal of psychology.

[107]  Edward A. Vessel,et al.  Perceptual Pleasure and the Brain , 2006 .

[108]  V. Gallese,et al.  Motion, emotion and empathy in esthetic experience , 2007, Trends in Cognitive Sciences.

[109]  M. Burke The neuroaesthetics of prose fiction: pitfalls, parameters and prospects , 2015, Front. Hum. Neurosci..

[110]  Helmut Leder,et al.  Next steps in neuroaesthetics: Which processes and processing stages to study? , 2013 .

[111]  H. Leder,et al.  Aesthetic emotions to art - What they are and what makes them special: Comment on "The quartet theory of human emotions: An integrative and neurofunctional model" by S. Koelsch et al. , 2015, Physics of life reviews.

[112]  Anjan Chatterjee,et al.  Prospects for a cognitive neuroscience of visual aesthetics , 2003 .

[113]  Florian Hutzler,et al.  Reverse inference is not a fallacy per se: Cognitive processes can be inferred from functional imaging data , 2014, NeuroImage.

[114]  V. Gallese,et al.  Out of touch with reality? Social perception in first-episode schizophrenia. , 2013, Social cognitive and affective neuroscience.

[115]  Vittorio Gallese,et al.  Functional organization of the insula and inner perisylvian regions , 2012, Proceedings of the National Academy of Sciences.

[116]  Di Dio Cinzia,et al.  Neuroaesthetics: a review , 2009, Current Opinion in Neurobiology.

[117]  Derek Hoiem,et al.  Action Recognition , 2014, Computer Vision, A Reference Guide.

[118]  Malin Björnsdotter,et al.  Vicarious Responses to Social Touch in Posterior Insular Cortex Are Tuned to Pleasant Caressing Speeds , 2011, The Journal of Neuroscience.

[119]  S. Zeki,et al.  Neural correlates of beauty. , 2004, Journal of neurophysiology.

[120]  Alice Mado Proverbio,et al.  Observation of Static Pictures of Dynamic Actions Enhances the Activity of Movement-Related Brain Areas , 2009, PloS one.

[121]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[122]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[123]  L. Chen Imaging of Pain , 2007, International anesthesiology clinics.

[124]  P. Haggard,et al.  Extrastriate body area underlies aesthetic evaluation of body stimuli , 2010, Experimental Brain Research.

[125]  E. Tulving Episodic memory: from mind to brain. , 2002, Annual review of psychology.

[126]  Maurizio Corbetta,et al.  Attention to Memory and the Environment: Functional Specialization and Dynamic Competition in Human Posterior Parietal Cortex , 2010, The Journal of Neuroscience.

[127]  M. Baulac,et al.  Functional anatomy of the insula: new insights from imaging , 2003, Surgical and Radiologic Anatomy.

[128]  A. Crawley,et al.  Viewing artworks: Contributions of cognitive control and perceptual facilitation to aesthetic experience , 2009, Brain and Cognition.

[129]  Wim Vanduffel,et al.  Grasping-Related Functional Magnetic Resonance Imaging Brain Responses in the Macaque Monkey , 2011, The Journal of Neuroscience.

[130]  Leonardo Fogassi,et al.  Motor functions of the parietal lobe , 2005, Current Opinion in Neurobiology.

[131]  Steven C. Bourassa Toward a theory of landscape aesthetics , 1988 .

[132]  Edward A. Vessel,et al.  The neural basis of scene preferences , 2007, Neuroreport.

[133]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[134]  G. Luppino,et al.  Anatomical Evidence for the Involvement of the Macaque Ventrolateral Prefrontal Area 12r in Controlling Goal-Directed Actions , 2011, The Journal of Neuroscience.