The Brain Network for Haptic Object Recogniton

Humans can haptically identify common three-dimensional objects surprisingly well. What are the neural mechanisms underlying this ability? Previous neuroimaging studies have shown that haptic object recognition involves a distributed network of brain regions beyond the conventional somatosensory cortices. However, the relative contributions of these regions to haptic object recognition are not well understood. In this chapter, I discuss three key hypotheses concerning the brain network underlying haptic object processing and its interaction with visual object processing. The first is that the occipito-temporal cortex, which has been considered to be part of the conventional visual cortex, plays a critical role in the haptic identification of common objects. The second is that distinct brain regions are involved in the haptic processing of two types of feature used for object identification: macro-geometric (e.g., shape) and material (e.g., roughness) properties. The third is that different brain regions are also involved in the visuo-haptic interaction of macro-geometric and material properties. Finally, I discuss some issues that remain to be addressed in future studies.

[1]  R L Klatzky,et al.  Identifying objects by touch: An “expert system” , 1985, Perception & psychophysics.

[2]  E T Rolls,et al.  Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. , 2003, Cerebral cortex.

[3]  E. Deibert,et al.  Neural pathways in tactile object recognition , 1999, Neurology.

[4]  D. Keltner,et al.  Touch communicates distinct emotions. , 2006, Emotion.

[5]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[6]  Susan J. Lederman,et al.  Functional Specialization and Convergence in the Occipito-temporal Cortex Supporting Haptic and Visual Identification of Human Faces and Body Parts: An fMRI Study , 2009, Journal of Cognitive Neuroscience.

[7]  H. Tanabe,et al.  Ventrolateral prefrontal cortex activity associated with individual differences in arbitrary delayed paired-association learning performance: A functional magnetic resonance imaging study , 2009, Neuroscience.

[8]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[9]  Michael S Beauchamp,et al.  See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex , 2005, Current Opinion in Neurobiology.

[10]  Y. Miyashita,et al.  Callosal window between prefrontal cortices: cognitive interaction to retrieve long-term memory. , 1998, Science.

[11]  R. Fleming Visual perception of materials and their properties , 2014, Vision Research.

[12]  Magdalena G. Wutte,et al.  Modality-Independent Coding of Spatial Layout in the Human Brain , 2011, Current Biology.

[13]  Susan J. Lederman,et al.  Multisensory Activation of the Intraparietal Area When Classifying Grating Orientation: A Functional Magnetic Resonance Imaging Study , 2006, The Journal of Neuroscience.

[14]  L. Cohen,et al.  A Ventral Visual Stream Reading Center Independent of Visual Experience , 2012, Current Biology.

[15]  Edmund T. Rolls,et al.  Warm pleasant feelings in the brain , 2008, NeuroImage.

[16]  Xiaoping Hu,et al.  Tactile discrimination of grating orientation: fMRI activation patterns , 2005, Human brain mapping.

[17]  M. Honda,et al.  Behavioral / Systems / Cognitive Functionally Segregated Neural Substrates for Arbitrary Audiovisual Paired-Association Learning , 2005 .

[18]  M. Costantini,et al.  Haptic perception and body representation in lateral and medial occipito-temporal cortices , 2011, Neuropsychologia.

[19]  Amir Amedi,et al.  Multisensory visual–tactile object related network in humans: insights gained using a novel crossmodal adaptation approach , 2009, Experimental Brain Research.

[20]  J. Wessberg,et al.  Discriminative and Affective Touch: Sensing and Feeling , 2014, Neuron.

[21]  Ravi S. Menon,et al.  Haptic study of three-dimensional objects activates extrastriate visual areas , 2002, Neuropsychologia.

[22]  Randall Stilla,et al.  Selective visuo‐haptic processing of shape and texture , 2008, Human brain mapping.

[23]  C. Price,et al.  Integrating Visual and Tactile Information in the Perirhinal Cortex , 2009, Cerebral cortex.

[24]  K. Zilles,et al.  Hierarchical Processing of Tactile Shape in the Human Brain , 2001, Neuron.

[25]  Susan J. Lederman,et al.  Tactile estimation of the roughness of gratings yields a graded response in the human brain: an fMRI study , 2005, NeuroImage.

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

[27]  J. Taylor,et al.  Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. , 1999, Brain : a journal of neurology.

[28]  Tim Shallice,et al.  Time-Dependent Changes in Learning Audiovisual Associations: A Single-Trial fMRI Study , 2000, NeuroImage.

[29]  T. James,et al.  The neural basis of haptic object processing. , 2007, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[30]  P Servos,et al.  fMRI-derived cortical maps for haptic shape, texture, and hardness. , 2001, Brain research. Cognitive brain research.

[31]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[32]  Riitta Hari,et al.  Audiovisual Integration of Letters in the Human Brain , 2000, Neuron.

[33]  R. Campbell,et al.  Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex , 2000, Current Biology.

[34]  Manabu Honda,et al.  Tactile–visual integration in the posterior parietal cortex: A functional magnetic resonance imaging study , 2008, Brain Research Bulletin.

[35]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[36]  Hartwig R. Siebner,et al.  Vision holds a greater share in visuo-haptic object recognition than touch , 2013, NeuroImage.

[37]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[38]  Xiaoping Hu,et al.  Activity and effective connectivity of parietal and occipital cortical regions during haptic shape perception , 2007, Neuropsychologia.

[39]  N. Kanwisher,et al.  The Human Body , 2001 .

[40]  G. Ekman,et al.  ROUGHNESS, SMOOTHNESS, AND PREFERENCE: A STUDY OF QUANTITATIVE RELATIONS IN INDIVIDUAL SUBJECTS. , 1965, Journal of experimental psychology.

[41]  G. Weniger,et al.  Impaired associative memory in temporal lobe epilepsy subjects after lesions of hippocampus, parahippocampal gyrus, and amygdala , 2004, Hippocampus.

[42]  Y. Miyashita,et al.  Backward spreading of memory-retrieval signal in the primate temporal cortex. , 2001, Science.

[43]  P E Roland,et al.  Cross-Modal Transfer of Information between the Tactile and the Visual Representations in the Human Brain: A Positron Emission Tomographic Study , 1998, The Journal of Neuroscience.

[44]  R. Klatzky,et al.  Haptic Recognition of Static and Dynamic Expressions of Emotion in the Live Face , 2007, Psychological science.

[45]  P. Roland,et al.  Shape and roughness activate different somatosensory areas in the human brain. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[47]  Susan J. Lederman,et al.  Brain networks involved in haptic and visual identification of facial expressions of emotion: An fMRI study , 2010, NeuroImage.

[48]  James K. Kroger,et al.  Cross-modal and cross-temporal association in neurons of frontal cortex , 2000, Nature.

[49]  Jeffrey M Yau,et al.  Representation of tactile curvature in macaque somatosensory area 2. , 2013, Journal of neurophysiology.

[50]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[51]  Norihiro Sadato,et al.  Role of the precuneus in the detection of incongruency between tactile and visual texture information: A functional MRI study , 2014, Neuropsychologia.

[52]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[53]  R. Klatzky,et al.  Relative availability of surface and object properties during early haptic processing. , 1997, Journal of experimental psychology. Human perception and performance.

[54]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[55]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[56]  Thomas W James,et al.  Enhanced effectiveness in visuo‐haptic object‐selective brain regions with increasing stimulus salience , 2009, Human brain mapping.

[57]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[58]  M. Cabanac,et al.  The perception of thermal comfort , 1965 .

[59]  M. Attia,et al.  Thermal pleasantness sensation: an indicator of thermal stress , 1982, European Journal of Applied Physiology and Occupational Physiology.

[60]  Kazuyuki Kanosue,et al.  Regional differences in temperature sensation and thermal comfort in humans. , 2008, Journal of applied physiology.

[61]  Norihiro Sadato,et al.  Tactile-visual cross-modal shape matching: a functional MRI study. , 2003, Brain research. Cognitive brain research.

[62]  Norihiro Sadato,et al.  Tactile Perception of Nonpainful Unpleasantness in Relation to Perceived Roughness: Effects of Inter-Element Spacing and Speed of Relative Motion of Rigid 2-D Raised-Dot Patterns at Two Body Loci , 2012, Perception.

[63]  Fiona N. Newell,et al.  Vision and touch: Independent or integrated systems for the perception of texture? , 2008, Brain Research.

[64]  John W. Lane,et al.  Receptive Field Properties of the Macaque Second Somatosensory Cortex: Representation of Orientation on Different Finger Pads , 2006, The Journal of Neuroscience.

[65]  G. Mower Perceived intensity of peripheral thermal stimuli is independent of internal body temperature. , 1976, Journal of comparative and physiological psychology.

[66]  El-Mehdi Meftah,et al.  Central neural mechanisms contributing to the perception of tactile roughness , 2002, Behavioural Brain Research.

[67]  Ryo Kitada,et al.  Haptic face processing. , 2007, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[68]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[69]  M. Hallett,et al.  Functional relevance of cross-modal plasticity in blind humans , 1997, Nature.

[70]  Xiaoping Hu,et al.  Dual pathways for haptic and visual perception of spatial and texture information , 2011, NeuroImage.

[71]  N. Sadato,et al.  The Brain Network Underlying the Recognition of Hand Gestures in the Blind: The Supramodal Role of the Extrastriate Body Area , 2014, The Journal of Neuroscience.

[72]  R. Klatzky,et al.  Hand movements: A window into haptic object recognition , 1987, Cognitive Psychology.

[73]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[74]  Y. Lamarre,et al.  Unmyelinated tactile afferents signal touch and project to insular cortex , 2002, Nature Neuroscience.

[75]  H Burton,et al.  Neuronal activity in the primary somatosensory cortex in monkeys (Macaca mulatta) during active touch of textured surface gratings: responses to groove width, applied force, and velocity of motion. , 1991, Journal of neurophysiology.

[76]  Rainer Goebel,et al.  Crossmodal interactions of haptic and visual texture information in early sensory cortex , 2013, NeuroImage.

[77]  K. Zilles,et al.  Crossmodal Processing of Object Features in Human Anterior Intraparietal Cortex An fMRI Study Implies Equivalencies between Humans and Monkeys , 2002, Neuron.

[78]  Michael X. Cohen,et al.  Inferior Temporal, Prefrontal, and Hippocampal Contributions to Visual Working Memory Maintenance and Associative Memory Retrieval , 2004, The Journal of Neuroscience.

[79]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[80]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[81]  Paul E. Downing,et al.  Crossmodal and action-specific: neuroimaging the human mirror neuron system , 2013, Trends in Cognitive Sciences.

[82]  P. Hagoort,et al.  The suppression of repetition enhancement: A review of fMRI studies , 2013, Neuropsychologia.