Integration of vibrotactile frequency information beyond the mechanoreceptor channel and somatotopy

A wide variety of tactile sensations arise from the activation of several types of mechanoreceptor-afferent channels scattered all over the body, and their projections create a somatotopic map in the somatosensory cortex. Recent findings challenge the traditional view that tactile signals from different mechanoreceptor-channels/locations are independently processed in the brain, though the contribution of signal integration to perception remains obscure. Here we show that vibrotactile frequency perception is functionally enriched by signal integration across different mechanoreceptor channels and separate skin locations. When participants touched two sinusoidal vibrations of far-different frequency, which dominantly activated separate channels with the neighboring fingers or the different hand and judged the frequency of one vibration, the perceived frequency shifted toward the other (assimilation effect). Furthermore, when the participants judged the frequency of the pair as a whole, they consistently reported an intensity-based interpolation of the two vibrations (averaging effect). Both effects were similar in magnitude between the same and different hand conditions and significantly diminished by asynchronous presentation of the vibration pair. These findings indicate that human tactile processing is global and flexible in that it can estimate the ensemble property of a large-scale tactile event sensed by various receptors distributed over the body.

[1]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

[2]  H. Hämäläinen,et al.  Vibrotactile thresholds during background vibration of long duration , 1981 .

[3]  R. Johansson,et al.  Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. , 1984, Human neurobiology.

[4]  J. F. Dammann,et al.  Temporal Frequency Channels Are Linked across Audition and Touch , 2009, Current Biology.

[5]  John Cohen The World of Touch , 1952, Nature.

[6]  H Burton,et al.  Neuronal activity in the second somatosensory cortex of monkeys (Macaca mulatta) during active touch of gratings. , 1993, Journal of neurophysiology.

[7]  S. Kitazawa,et al.  Reversal of subjective temporal order due to arm crossing , 2001, Nature Neuroscience.

[8]  D. Levi Crowding—An essential bottleneck for object recognition: A mini-review , 2008, Vision Research.

[9]  George A. Gescheider,et al.  Vibrotactile masking: Effects of oneand two-site stimulation , 1983, Perception & psychophysics.

[10]  Nicholas P. Holmes,et al.  Within, but not between hands interactions in vibrotactile detection thresholds reflect somatosensory receptive field organization , 2014, Front. Psychol..

[11]  R. LaMotte,et al.  Fine-scale organization of SI (area 3b) in the squirrel monkey revealed with intrinsic optical imaging. , 2001, Journal of neurophysiology.

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

[13]  W W Sutherling,et al.  Cortical sensory representation of the human hand , 1992, Neurology.

[14]  O. Hikosaka,et al.  Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey , 1983, Experimental Brain Research.

[15]  Jürgen Konczak,et al.  Interaction of finger representation in the human first somatosensory cortex: a neuromagnetic study , 1998, Neuroscience Letters.

[16]  John H. Wright,et al.  Information-Processing Channels in the Tactile Sensory System: A Psychophysical and Physiological Analysis , 2008 .

[17]  S. C. Gandevia,et al.  Convergence in the somatosensory pathway between cutaneous afferents from the index and middle fingers in man , 2004, Experimental Brain Research.

[18]  Junji Watanabe,et al.  Contribution of within- and cross-channel information to vibrotactile frequency discrimination , 2013, Brain Research.

[19]  G. Alvarez Representing multiple objects as an ensemble enhances visual cognition , 2011, Trends in Cognitive Sciences.

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

[21]  Li Min Chen,et al.  Modality maps within primate somatosensory cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Hannes P. Saal,et al.  Rate and timing of cortical responses driven by separate sensory channels , 2015, eLife.

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

[24]  P. Haggard,et al.  The Posterior Parietal Cortex Remaps Touch into External Space , 2010, Current Biology.

[25]  V. Ramachandran,et al.  The perception of phantom limbs , 1998 .

[26]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[27]  S. Soto-Faraco,et al.  Alleviating the ‘crossed-hands’ deficit by seeing uncrossed rubber hands , 2007, Experimental Brain Research.

[28]  M. Paré,et al.  Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey , 2002, The Journal of comparative neurology.

[29]  Laurence R. Harris,et al.  Contralateral tactile masking between forearms , 2013, Experimental Brain Research.

[30]  C. Spence,et al.  Tactile selective attention and body posture: Assessing the multisensory contributions of vision and proprioception , 2004, Perception & psychophysics.

[31]  Richard D. Gilson,et al.  Vibrotactile masking: Some spatial and temporal aspects , 1969 .

[32]  R. Johansson,et al.  Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements , 1982, Brain Research.

[33]  Jon Driver,et al.  Multimodal spatial constraints on tactile selective attention. , 1996 .

[34]  Astrid M. L. Kappers,et al.  Context effects in haptic perception of roughness , 2009, Experimental Brain Research.

[35]  G. Schott Penfield's homunculus: a note on cerebral cartography. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[36]  K. Sathian,et al.  Intermanual referral of sensation to anesthetic hands , 2000, Neurology.

[37]  Nigel H. Lovell,et al.  Convergence across Tactile Afferent Types in Primary and Secondary Somatosensory Cortices , 2014, PloS one.

[38]  S. Bolanowski,et al.  Four channels mediate the mechanical aspects of touch. , 1988, The Journal of the Acoustical Society of America.

[39]  Yoshitaka Nakajima,et al.  Auditory Scene Analysis: The Perceptual Organization of Sound Albert S. Bregman , 1992 .

[40]  John W. Lane,et al.  Receptive Field (RF) Properties of the Macaque Second Somatosensory Cortex: RF Size, Shape, and Somatotopic Organization , 2006, The Journal of Neuroscience.

[41]  D. Levi,et al.  Visual crowding: a fundamental limit on conscious perception and object recognition , 2011, Trends in Cognitive Sciences.

[42]  V. Mountcastle,et al.  Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibers innervating the monkey hand. , 1972, Journal of neurophysiology.

[43]  V. Ramachandran,et al.  The perception of phantom limbs. The D. O. Hebb lecture. , 1998, Brain : a journal of neurology.

[44]  J. Kaas,et al.  Modular segregation of functional cell classes within the postcentral somatosensory cortex of monkeys. , 1981, Science.

[45]  R. T. Verrillo,et al.  Effect of Contactor Area on the Vibrotactile Threshold , 1963 .

[46]  M. Rowe,et al.  Perceived pitch of vibrotactile stimuli: effects of vibration amplitude, and implications for vibration frequency coding. , 1990, The Journal of physiology.

[47]  M. Hollins,et al.  A ratio code for vibrotactile pitch. , 1998, Somatosensory & motor research.

[48]  J C Craig,et al.  Tactile attention and the perception of moving tactile stimuli , 1991, Perception & psychophysics.

[49]  W. Spencer,et al.  Mechanoreceptive submodality channel interactions: Psychophysical observations on differential activation of flutter and vibration , 1985, Brain Research.

[50]  C. Raggi,et al.  Mini review , 2004 .

[51]  Riitta Hari,et al.  Interaction between afferent input from fingers in human somatosensory cortex , 1995, Brain Research.

[52]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[53]  R. Andersen Encoding of intention and spatial location in the posterior parietal cortex. , 1995, Cerebral cortex.

[54]  J. Lund,et al.  Compulsory averaging of crowded orientation signals in human vision , 2001, Nature Neuroscience.

[55]  V. Mountcastle,et al.  Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. , 1975, Journal of neurophysiology.

[56]  Riitta Salmelin,et al.  Tactile information from the human hand reaches the ipsilateral primary somatosensory cortex , 1995, Neuroscience Letters.

[57]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[58]  F. Billmeyer Color Science: Concepts and Methods, Quantitative Data and Formulae, 2nd ed., by Gunter Wyszecki and W. S. Stiles, John Wiley and Sons, New York, 1982, 950 pp. Price: $75.00 , 1983 .