Preserved Object Weight Processing after Bilateral Lateral Occipital Complex Lesions

Object interaction requires knowledge of the weight of an object, as well as its shape. The lateral occipital complex (LOC), an area within the ventral visual pathway, is well known to be critically involved in processing visual shape information. Recently, however, LOC has also been implicated in coding object weight before grasping—a result that is surprising because weight is a nonvisual object property that is more relevant for motor interaction than visual perception. Here, we examined the causal role of LOC in perceiving heaviness and in determining appropriate fingertip forces during object lifting. We studied perceptions of heaviness and lifting behavior in a neuropsychological patient (M.C.) who has large bilateral occipitotemporal lesions that include LOC. We compared the patient's performance to a group of 18 neurologically healthy age-matched controls. Participants were asked to lift and report the perceived heaviness of a set of equally weighted spherical objects of various sizes—stimuli which typically induce the size–weight illusion, in which the smaller objects feel heavier than the larger objects despite having identical mass. Despite her ventral stream lesions, M.C. experienced a robust size–weight illusion induced by visual cues to object volume, and the magnitude of the illusion in M.C. was comparable to age-matched controls. Similarly, M.C. evinced predictive fingertip force scaling to visual size cues during her initial lifts of the objects that were well within the normal range. These single-case neuropsychological findings suggest that LOC is unlikely to play a causal role in computing object weight.

[1]  Jonathan S. Cant,et al.  Living in a material world: how visual cues to material properties affect the way that we lift objects and perceive their weight. , 2009, Journal of neurophysiology.

[2]  M. Goodale,et al.  The influence of competing perceptual and motor priors in the context of the size–weight illusion , 2010, Experimental Brain Research.

[3]  G. Riddoch DISSOCIATION OF VISUAL PERCEPTIONS DUE TO OCCIPITAL INJURIES, WITH ESPECIAL REFERENCE TO APPRECIATION OF MOVEMENT , 1917 .

[4]  Charpentier's Papers of 1886 and 1891 on Weight Perception and the Size-Weight Illusion , 2012, Perceptual and motor skills.

[5]  G. Buckingham,et al.  The Influence of Prior Knowledge on Perception and Action: Relationships to Autistic Traits , 2016, Journal of autism and developmental disorders.

[6]  S. Lacey,et al.  Visuo-haptic multisensory object recognition, categorization, and representation , 2014, Front. Psychol..

[7]  Louise P. Kirsch,et al.  Information about the Weight of Grasped Objects from Vision and Internal Models Interacts within the Primary Motor Cortex , 2010, The Journal of Neuroscience.

[8]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[9]  J. Randall Flanagan,et al.  Representation of Object Weight in Human Ventral Visual Cortex , 2014, Current Biology.

[10]  D. Westwood,et al.  Opposite perceptual and sensorimotor responses to a size-weight illusion. , 2006, Journal of neurophysiology.

[11]  Melvyn A. Goodale,et al.  Size Matters: A Single Representation Underlies Our Perceptions of Heaviness in the Size-Weight Illusion , 2013, PloS one.

[12]  David C. Plaut,et al.  ‘What’ Is Happening in the Dorsal Visual Pathway , 2016, Trends in Cognitive Sciences.

[13]  B. Wandell,et al.  The vertical occipital fasciculus: A century of controversy resolved by in vivo measurements , 2014, Proceedings of the National Academy of Sciences.

[14]  S. C. Masin,et al.  Experimental demonstration of the sensory basis of the size-weight illusion , 1988, Perception & psychophysics.

[15]  Markus Graf,et al.  When Action Observation Facilitates Visual Perception: Activation in Visuo-Motor Areas Contributes to Object Recognition. , 2015, Cerebral cortex.

[16]  H. Forssberg,et al.  Lighter or Heavier Than Predicted: Neural Correlates of Corrective Mechanisms during Erroneously Programmed Lifts , 2006, The Journal of Neuroscience.

[17]  Melvyn A. Goodale,et al.  Lifting without seeing: the role of vision in perceiving and acting upon the size‐weight illusion , 2010 .

[18]  M. Jeannerod,et al.  Human Brain Activity Related to the Perception of Spatial Features of Objects , 1999, NeuroImage.

[19]  R. Johansson,et al.  Visual size cues in the programming of manipulative forces during precision grip , 2004, Experimental Brain Research.

[20]  G. Buckingham Getting a grip on heaviness perception: a review of weight illusions and their probable causes , 2014, Experimental Brain Research.

[21]  M. Goodale,et al.  Two visual pathways – Where have they taken us and where will they lead in future? , 2018, Cortex.

[22]  Melvyn A. Goodale,et al.  Dissociable neural mechanisms for determining the perceived heaviness of objects and the predicted weight of objects during lifting: An fMRI investigation of the size–weight illusion , 2009, NeuroImage.

[23]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[24]  Rainer Goebel,et al.  Psychophysical and neuroimaging responses to moving stimuli in a patient with the Riddoch phenomenon due to bilateral visual cortex lesions , 2019, Neuropsychologia.

[25]  Paul L Gribble,et al.  Does the sensorimotor system minimize prediction error or select the most likely prediction during object lifting? , 2017, Journal of neurophysiology.

[26]  Jacqueline C. Snow,et al.  What Role Does “Elongation” Play in “Tool-Specific” Activation and Connectivity in the Dorsal and Ventral Visual Streams? , 2018, Cerebral cortex.

[27]  D. C. Howell,et al.  Comparing an Individual's Test Score Against Norms Derived from Small Samples , 1998 .

[28]  Jennifer L. Milne,et al.  The Size-Weight Illusion Induced Through Human Echolocation , 2015, Psychological science.

[29]  J. Flanagan,et al.  Independence of perceptual and sensorimotor predictions in the size–weight illusion , 2000, Nature Neuroscience.

[30]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[31]  Paul H. Garthwaite,et al.  Statistical Methods for Single-Case Studies in Neuropsychology: Comparing the Slope of a Patient's Regression Line with those of a Control Sample , 2004, Cortex.

[32]  Philippe A. Chouinard,et al.  Role of the Primary Motor and Dorsal Premotor Cortices in the Anticipation of Forces during Object Lifting , 2005, The Journal of Neuroscience.

[33]  Sabine Kastner,et al.  The functional neuroanatomy of object agnosia: A case study , 2010 .

[34]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

[35]  Brian A. Wandell,et al.  The posterior arcuate fasciculus and the vertical occipital fasciculus , 2017, Cortex.

[36]  John H. R. Maunsell,et al.  Shape selectivity in primate lateral intraparietal cortex , 1998, Nature.

[37]  Peter Janssen,et al.  Posterior Parietal Cortex Drives Inferotemporal Activations During Three-Dimensional Object Vision , 2016, PLoS biology.

[38]  P. Garthwaite,et al.  Point and interval estimates of effect sizes for the case-controls design in neuropsychology: Rationale, methods, implementations, and proposed reporting standards , 2010, Cognitive neuropsychology.

[39]  Kalanit Grill-Spector,et al.  On object selectivity and the anatomy of the human fusiform gyrus , 2018, NeuroImage.

[40]  Jacqueline C. Snow,et al.  Preserved Haptic Shape Processing after Bilateral LOC Lesions , 2015, The Journal of Neuroscience.

[41]  C. M. Davis,et al.  Lifting movements in the size-weight illusion , 1976 .