Analysis of haptic information in the cerebral cortex.

Haptic sensing of objects acquires information about a number of properties. This review summarizes current understanding about how these properties are processed in the cerebral cortex of macaques and humans. Nonnoxious somatosensory inputs, after initial processing in primary somatosensory cortex, are partially segregated into different pathways. A ventrally directed pathway carries information about surface texture into parietal opercular cortex and thence to medial occipital cortex. A dorsally directed pathway transmits information regarding the location of features on objects to the intraparietal sulcus and frontal eye fields. Shape processing occurs mainly in the intraparietal sulcus and lateral occipital complex, while orientation processing is distributed across primary somatosensory cortex, the parietal operculum, the anterior intraparietal sulcus, and a parieto-occipital region. For each of these properties, the respective areas outside primary somatosensory cortex also process corresponding visual information and are thus multisensory. Consistent with the distributed neural processing of haptic object properties, tactile spatial acuity depends on interaction between bottom-up tactile inputs and top-down attentional signals in a distributed neural network. Future work should clarify the roles of the various brain regions and how they interact at the network level.

[1]  M. Srinivasan,et al.  Tactile discrimination of shape: responses of slowly and rapidly adapting mechanoreceptive afferents to a step indented into the monkey fingerpad , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  C. Spence,et al.  Audiotactile interactions in roughness perception , 2002, Experimental Brain Research.

[3]  D J Felleman,et al.  Somatotopic organization of the lateral sulcus of owl monkeys: Area 3b, s‐II, and a ventral somatosensory area , 1989, The Journal of comparative neurology.

[4]  Mandayam A. Srinivasan,et al.  Tactual discrimination of softness: abilities and mechanisms , 1996 .

[5]  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.

[6]  Claude Alain,et al.  Assessing the auditory dual-pathway model in humans , 2004, NeuroImage.

[7]  Bidhan Lamichhane,et al.  Oscillatory activity in neocortical networks during tactile discrimination near the limit of spatial acuity , 2014, NeuroImage.

[8]  Steven S. Hsiao,et al.  Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex , 2015, Neuron.

[9]  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.

[10]  M. Heller Texture perception in sighted and blind observers , 1989, Perception & psychophysics.

[11]  Mark Holliins,et al.  Perceptual dimensions of tactile surface texture: A multidimensional scaling analysis , 1993, Perception & psychophysics.

[12]  William M. Stern,et al.  Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex , 2007, Nature Neuroscience.

[13]  Melvyn A. Goodale,et al.  Are visual texture-selective areas recruited during haptic texture discrimination? , 2013, NeuroImage.

[14]  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.

[15]  David P. Friedman,et al.  Physiological evidence for serial processing in somatosensory cortex. , 1987, Science.

[16]  S. Lacey,et al.  Cross-Modal Object Recognition Is Viewpoint-Independent , 2007, PloS one.

[17]  James C Craig,et al.  Convergence of submodality-specific input onto neurons in primary somatosensory cortex. , 2009, Journal of neurophysiology.

[18]  J. Maunsell,et al.  State dependent activity in monkey visual cortex , 2004, Experimental Brain Research.

[19]  H. Freund,et al.  The role of the inferior parietal cortex in linking the tactile perception and manual construction of object shapes. , 2001, Cerebral cortex.

[20]  J. F. Dammann,et al.  The Representation of Stimulus Orientation in the Early Stages of Somatosensory Processing , 2008, The Journal of Neuroscience.

[21]  A. Goodwin,et al.  Representation of curved surfaces in responses of mechanoreceptive afferent fibers innervating the monkey's fingerpad , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  K. Sathian,et al.  Neural Changes with Tactile Learning Reflect Decision-Level Reweighting of Perceptual Readout , 2013, The Journal of Neuroscience.

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

[24]  G. T. Coleman,et al.  Hierarchical equivalence of somatosensory areas I and II for tactile processing in the cerebral cortex of the marmoset monkey. , 2001, Journal of neurophysiology.

[25]  K. Sathian,et al.  Multisensory cortical processing of object shape and its relation to mental imagery , 2004, Cognitive, affective & behavioral neuroscience.

[26]  Xiaoping Hu,et al.  Object familiarity modulates effective connectivity during haptic shape perception , 2010, NeuroImage.

[27]  Jessie Chen,et al.  Neurophysiology of prehension. III. Representation of object features in posterior parietal cortex of the macaque monkey. , 2007, Journal of neurophysiology.

[28]  Tingrui Pan,et al.  Reversible deactivation of higher-order posterior parietal areas. II. Alterations in response properties of neurons in areas 1 and 2. , 2014, Journal of neurophysiology.

[29]  R. Caselli,et al.  Ventrolateral and dorsomedial somatosensory association cortex damage produces distinct somesthetic syndromes in humans , 1993, Neurology.

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

[31]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[32]  Ehud Ahissar,et al.  Importance of Temporal Cues for Tactile Spatial- Frequency Discrimination , 2001, The Journal of Neuroscience.

[33]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[34]  Emiliano Ricciardi,et al.  Touching Motion: rTMS on the Human Middle Temporal Complex Interferes with Tactile Speed Perception , 2012, Brain Topography.

[35]  M. Hollins,et al.  Evidence for the duplex theory of tactile texture perception , 2000, Perception & psychophysics.

[36]  A. Goodwin,et al.  Encoding of object curvature by tactile afferents from human fingers. , 1997, Journal of neurophysiology.

[37]  Tingrui Pan,et al.  Reversible deactivation of higher-order posterior parietal areas. I. Alterations of receptive field characteristics in early stages of neocortical processing. , 2014, Journal of neurophysiology.

[38]  C. Galletti,et al.  Functional Properties of Neurons in the Anterior Bank of the Parieto‐occipital Sulcus of the Macaque Monkey , 1991, The European journal of neuroscience.

[39]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

[40]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[41]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  M. Srinivasan,et al.  Tactual discrimination of softness. , 1995, Journal of neurophysiology.

[43]  Simon Lacey,et al.  Object familiarity modulates the relationship between visual object imagery and haptic shape perception , 2010, NeuroImage.

[44]  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.

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

[46]  Forrest W. Young,et al.  Individual differences in perceptual space for tactile textures: Evidence from multidimensional scaling , 2000, Perception & psychophysics.

[47]  John W. Lane,et al.  Representation of orientation in the somatosensory system , 2002, Behavioural Brain Research.

[48]  D. Goldreich,et al.  Tactile Spatial Acuity Enhancement in Blindness: Evidence for Experience-Dependent Mechanisms , 2011, The Journal of Neuroscience.

[49]  Minming Zhang,et al.  Neural networks active during tactile form perception: common and differential activity during macrospatial and microspatial tasks. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[50]  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.

[51]  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.

[52]  K. O. Johnson,et al.  Tactile spatial resolution. III. A continuum mechanics model of skin predicting mechanoreceptor responses to bars, edges, and gratings. , 1981, Journal of neurophysiology.

[53]  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.

[54]  J. Fuster,et al.  Unit activity in monkey parietal cortex related to haptic perception and temporary memory , 2004, Experimental Brain Research.

[55]  M. Srinivasan,et al.  Tactile discrimination of shape: responses of slowly adapting mechanoreceptor afferents to a step stroked across the monkey fingerpad , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  Randall Stilla,et al.  Spatial imagery in haptic shape perception , 2014, Neuropsychologia.

[57]  K. Sathian,et al.  Tactile spatial acuity at the human fingertip and lip , 1996, Neurology.

[58]  Pramodsingh H Thakur,et al.  Second-order receptive fields reveal multidigit interactions in area 3b of the macaque monkey. , 2012, Journal of neurophysiology.

[59]  K. Sathian,et al.  Altered responses to cutaneous stimuli in the second somatosensory cortex following lesions of the postcentral gyrus in infant and juvenile macaques , 1990, The Journal of comparative neurology.

[60]  Scott T. Grafton,et al.  Feeling with the mind's eye , 1997, Neuroreport.

[61]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[62]  Jeffrey M Yau,et al.  Analogous intermediate shape coding in vision and touch , 2009, Proceedings of the National Academy of Sciences.

[63]  John J. Foxe,et al.  Tactile shape discrimination recruits human lateral occipital complex during early perceptual processing , 2010, Human brain mapping.

[64]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[65]  K. Zilles,et al.  t Object Shape Differences Reflected by Somatosensory Cortical Activation , 2000, The Journal of Neuroscience.

[66]  G. Essick,et al.  Tactile motion activates the human middle temporal/V5 (MT/V5) complex , 2002, The European journal of neuroscience.

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

[68]  J. Craig,et al.  Shape Invariant Coding of Motion Direction in Somatosensory Cortex , 2010, PLoS biology.

[69]  K. O. Johnson,et al.  Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. , 1981, Journal of neurophysiology.

[70]  John R. Votaw,et al.  Task-specific recruitment of dorsal and ventral visual areas during tactile perception , 2004, Neuropsychologia.

[71]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[72]  J. Duhamel,et al.  Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey , 2007, The Journal of Neuroscience.

[73]  Xiaoping Hu,et al.  Posteromedial Parietal Cortical Activity and Inputs Predict Tactile Spatial Acuity , 2007, The Journal of Neuroscience.

[74]  Kenneth M. Heilman,et al.  Multimodal agnosia after unilateral left hemisphere lesion , 1986, Neurology.

[75]  Amir Amedi,et al.  Combined activation and deactivation of visual cortex during tactile sensory processing. , 2007, Journal of neurophysiology.

[76]  Tony Ro,et al.  Human MST But Not MT Responds to Tactile Stimulation , 2007, The Journal of Neuroscience.

[77]  S. Hsiao,et al.  Representation of object size in the somatosensory system. , 2006, Journal of neurophysiology.

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

[79]  G. Lakoff,et al.  Metaphors We Live By , 1980 .

[80]  Vincent Hayward,et al.  Motion Aftereffects Transfer between Touch and Vision , 2009, Current Biology.

[81]  Christopher R. Stambaugh,et al.  Simultaneous encoding of tactile information by three primate cortical areas , 1998, Nature Neuroscience.

[82]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[83]  P. Roland,et al.  Somatosensory Activations of the Parietal Operculum of Man. A PET Study , 1995, The European journal of neuroscience.

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

[85]  Volkmar Glauche,et al.  Localization of human intraparietal areas AIP, CIP, and LIP using surface orientation and saccadic eye movement tasks , 2008, Human brain mapping.

[86]  E. Chudler,et al.  Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. , 1994, Journal of neurophysiology.

[87]  C. Büchel,et al.  Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: an event-related fMRI study. , 2001, Journal of neurophysiology.

[88]  John W. Lane,et al.  Receptive Field Properties of the Macaque Second Somatosensory Cortex: Nonlinear Mechanisms Underlying the Representation of Orientation Within a Finger Pad , 2006, The Journal of Neuroscience.

[89]  K. Sathian,et al.  Tactile sensing of surface features , 1989, Trends in Neurosciences.

[90]  Kenneth O. Johnson,et al.  Neural Mechanisms of Tactual form and Texture Perception , 1992 .

[91]  K. Sathian,et al.  Temporal Cues Contribute to Tactile Perception of Roughness , 2001, The Journal of Neuroscience.

[92]  R. Klatzky,et al.  There's more to touch than meets the eye: The salience of object attributes for haptics with and without vision. , 1987 .

[93]  Guy Marchal,et al.  Passive somatosensory discrimination tasks in healthy volunteers: Differential networks involved in familiar versus unfamiliar shape and length discrimination , 2005, NeuroImage.

[94]  Felix Blankenburg,et al.  Tactile and visual motion direction processing in hMT+/V5 , 2014, NeuroImage.

[95]  C. Galletti,et al.  Wide-Field Retinotopy Defines Human Cortical Visual Area V6 , 2006, The Journal of Neuroscience.

[96]  Michael L. Lipton,et al.  Ipsilateral Hand Input to Area 3b Revealed by Converging Hemodynamic and Electrophysiological Analyses in Macaque Monkeys , 2006, The Journal of Neuroscience.

[97]  S. Lacey,et al.  Perceptual learning of view-independence in visuo-haptic object representations , 2009, Experimental Brain Research.

[98]  Jamie L. Reed,et al.  Neurophysiology of Tactile Perception : A Tribute to Steven Hsiao Chronic recordings reveal tactile stimuli can suppress spontaneous activity of neurons in somatosensory cortex of awake and anesthetized primates , 2016 .

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

[100]  M. Sereno,et al.  A human parietal face area contains aligned head-centered visual and tactile maps , 2006, Nature Neuroscience.

[101]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[102]  J. Semmes,et al.  Behavioral consequences of selective subtotal ablations in the postcentral gyrus of Macaca mulatta. , 1974, Brain research.

[103]  Kenith V. Sobel,et al.  PSYCHOLOGICAL SCIENCE Research Article Neural Synergy Between Kinetic Vision and Touch , 2022 .

[104]  Y. Iwamura Hierarchical somatosensory processing , 1998, Current Opinion in Neurobiology.

[105]  Ian R Summers,et al.  A functional-magnetic-resonance-imaging investigation of cortical activation from moving vibrotactile stimuli on the fingertip. , 2009, The Journal of the Acoustical Society of America.

[106]  A. Goodwin,et al.  Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[107]  M J Farah,et al.  Tactile agnosia. Underlying impairment and implications for normal tactile object recognition. , 1996, Brain : a journal of neurology.

[108]  S S Hsiao,et al.  Spatial pattern representation and transformation in monkey somatosensory cortex. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[109]  C. Spence,et al.  Tactile dominance in speeded discrimination of textures , 2003, Experimental Brain Research.

[110]  Elisabeth A. Murray,et al.  Relative contributions of SII and area 5 to tactile discrimination in monkeys , 1984, Behavioural Brain Research.

[111]  A. Goodwin,et al.  Human tactile discrimination of curvature when contact area with the skin remains constant , 2005, Experimental Brain Research.

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

[113]  Kenneth O. Johnson,et al.  Spatiotemporal Receptive Fields of Peripheral Afferents and Cortical Area 3b and 1 Neurons in the Primate Somatosensory System , 2006, The Journal of Neuroscience.

[114]  Justine Cléry,et al.  Whole brain mapping of visual and tactile convergence in the macaque monkey , 2015, NeuroImage.

[115]  Leah Krubitzer,et al.  Organization of area 3a in macaque monkeys: Contributions to the cortical phenotype , 2004, The Journal of comparative neurology.

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

[117]  Gereon R Fink,et al.  The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. , 2007, Cerebral cortex.

[118]  Simon Lacey,et al.  Crossmodal and multisensory interactions between vision and touch , 2015, Scholarpedia.

[119]  K Sathian,et al.  Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[120]  Shy Shoham,et al.  Neural substrates of tactile object recognition: An fMRI study , 2004, Human brain mapping.

[121]  M. Srinivasan,et al.  Tactile discrimination of shape: responses of rapidly adapting mechanoreceptive afferents to a step stroked across the monkey fingerpad , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[122]  Harold Burton,et al.  Second Somatosensory Cortex and Related Areas , 1986 .

[123]  K. Zilles,et al.  Object shape differences reflected by somatosensory cortical activation in human , 2000 .

[124]  J. Haxby,et al.  The effect of visual experience on the development of functional architecture in hMT+. , 2007, Cerebral cortex.

[125]  Mareike M. Menz,et al.  Multisensory interactions between auditory and haptic object recognition. , 2013, Cerebral cortex.

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

[127]  John W. Lane,et al.  Receptive Field Properties of the Macaque Second Somatosensory Cortex: Evidence for Multiple Functional Representations , 2004, The Journal of Neuroscience.

[128]  J C Craig,et al.  The tactile perception of stimulus orientation , 2008, Somatosensory & motor research.

[129]  Scott T. Grafton,et al.  Involvement of visual cortex in tactile discrimination of orientation , 1999, Nature.

[130]  J. Craig,et al.  Neural Mechanisms of Tactile Motion Integration in Somatosensory Cortex , 2011, Neuron.

[131]  Roberta L. Klatzky,et al.  What vs. where in touch: an fMRI study , 2005, NeuroImage.

[132]  Amir Amedi,et al.  A Putative Model of Multisensory Object Representation , 2009, Brain Topography.

[133]  M Mishkin,et al.  Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. , 1992, Journal of neurophysiology.

[134]  D. Eagleman,et al.  Evidence against the temporal subsampling account of illusory motion reversal. , 2008, Journal of vision.

[135]  K Sathian,et al.  Feeling with the mind's eye: the role of visual imagery in tactile perception. , 2001, Optometry and vision science : official publication of the American Academy of Optometry.

[136]  J. Kaas,et al.  Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. , 2009, Cerebral cortex.

[137]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[138]  Leslie G. Ungerleider,et al.  Tactile form and location processing in the human brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[139]  Gregor Thut,et al.  Feeling by Sight or Seeing by Touch? , 2004, Neuron.

[140]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

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

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

[143]  Synnöve Carlson,et al.  Multisensory Integration of Sounds and Vibrotactile Stimuli in Processing Streams for “What” and “Where” , 2009, The Journal of Neuroscience.

[144]  T. Hendler,et al.  Convergence of visual and tactile shape processing in the human lateral occipital complex. , 2002, Cerebral cortex.

[145]  Xiaoping Hu,et al.  Neural processing underlying tactile microspatial discrimination in the blind: a functional magnetic resonance imaging study. , 2008, Journal of vision.

[146]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[147]  Sliman J. Bensmaia,et al.  Texture from touch , 2009, Scholarpedia.

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

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

[150]  Ross M. VanDerKlok,et al.  Shape from sound: Evidence for a shape operator in the lateral occipital cortex , 2011, Neuropsychologia.

[151]  Ryuta Kawashima,et al.  A PET Study of Somatosensory Discrimination in Man. Microgeometry Versus Macrogeometry , 1994, The European journal of neuroscience.

[152]  Michael S. Beauchamp,et al.  Re-examining overlap between tactile and visual motion responses within hMT+ and STS , 2015, NeuroImage.

[153]  J. A. Pruszynski,et al.  Edge-orientation processing in first-order tactile neurons , 2014, Nature Neuroscience.

[154]  Randall Stilla,et al.  Metaphorically feeling: Comprehending textural metaphors activates somatosensory cortex , 2012, Brain and Language.

[155]  Giuseppe Casaceli,et al.  Four-dimensional maps of the human somatosensory system , 2016, Proceedings of the National Academy of Sciences.

[156]  Hannes P. Saal,et al.  Spatial and temporal codes mediate the tactile perception of natural textures , 2014, 2014 IEEE Haptics Symposium (HAPTICS).

[157]  Per E. Roland,et al.  Somatosensory detection of microgeometry, macrogeometry and kinesthesia after localized lesions of the cerebral hemispheres in man , 1987, Brain Research Reviews.

[158]  Cristina Simões-Franklin,et al.  Active and passive touch differentially activate somatosensory cortex in texture perception , 2011, Human brain mapping.

[159]  K O Johnson,et al.  The limit of tactile spatial resolution in humans , 1994, Neurology.