Edge-orientation processing in first-order tactile neurons

Nature Neuroscience

Volumn 17, Issue 10, 2014, Pages 1404-1409

  Pruszynski, J Andrew ^a   Johansson, Roland S ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ARTICLE; BRAIN CORTEX; GLABROUS SKIN; HUMAN; NERVE CELL; NERVE FIBER; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; RECEPTIVE FIELD; STIMULUS RESPONSE; TACTILE DISCRIMINATION; TACTILE STIMULATION; TOUCH; VISION; VISUAL SYSTEM; ADULT; BIOLOGICAL MODEL; BRAIN MAPPING; CYTOLOGY; FEMALE; MALE; MOVEMENT PERCEPTION; PHYSIOLOGY; PREDICTIVE VALUE; RECEIVER OPERATING CHARACTERISTIC; SENSORY NERVE; SOMATOSENSORY CORTEX; TIME; YOUNG ADULT;

ACTION POTENTIALS; ADULT; AFFERENT PATHWAYS; BRAIN MAPPING; FEMALE; HUMANS; MALE; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NEURONS; ORIENTATION; PREDICTIVE VALUE OF TESTS; ROC CURVE; SOMATOSENSORY CORTEX; TIME FACTORS; TOUCH; YOUNG ADULT;

EID: 84921711696     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3804     Document Type: Article

References (50)

1. Bensmaia, S.J., Denchev, P.V., Dammann, J.F., Craig, J.C. & Hsiao, S.S. The representation of stimulus orientation in the early stages of somatosensory processing. J. Neurosci. 28, 776-786 (2008).
2. Yau, J.M., Pasupathy, A., Fitzgerald, P.J., Hsiao, S.S. & Connor, C.E. Analogous intermediate shape coding in vision and touch. Proc. Natl. Acad. Sci. USA 106, 16457-16462 (2009).
3. Fitzgerald, P.J., Lane, J.W., Thakur, P.H. & Hsiao, S.S. Receptive field properties of the macaque second somatosensory cortex: representation of orientation on different finger pads. J. Neurosci. 26, 6473-6484 (2006).
4. Hubel, D.H. & Wiesel, T.N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215-243 (1968).
5. Shapley, R., Hawken, M. & Ringach, D.L. Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38, 689-699 (2003).
6. Hsiao, S. Central mechanisms of tactile shape perception. Curr. Opin. Neurobiol. 18, 418-424 (2008).
7. Ferster, D. & Miller, K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441-471 (2000).
8. Gollisch, T. & Meister, M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65, 150-164 (2010).
9. Venkataramani, S. & Taylor, W.R. Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition. J. Neurosci. 30, 15664-15676 (2010).
10. Cauna, N. Nerve supply and nerve endings in Meissners corpuscles. Am. J. Anat. 99, 315-350 (1956).
11. Looft, F.J. Response of cat cutaneous mechanoreceptors to punctate and grating stimuli. J. Neurophysiol. 56, 208-220 (1986).
12. Paré, M., Smith, A.M. & Rice, F.L. Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey. J. Comp. Neurol. 445, 347-359 (2002).
13. Goldfinger, M.D. Random-sequence stimulation of the G1 hair afferent unit. Somatosens. Mot. Res. 7, 19-45 (1990).
14. Brown, A.G. & Iggo, A. A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit. J. Physiol. (Lond.) 193, 707-733 (1967).
15. Lesniak, D.R. et al. Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors. eLife (Cambridge) 3, e01488 (2014).
16. Vallbo, A.B., Olausson, H., Wessberg, J. & Kakuda, N. Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. J. Physiol. (Lond.) 483, 783-795 (1995).
17. Johansson, R.S. Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. J. Physiol. (Lond.) 281, 101-125 (1978).
18. Phillips, J.R., Johansson, R.S. & Johnson, K.O. Responses of human mechanoreceptive afferents to embossed dot arrays scanned across fingerpad skin. J. Neurosci. 12, 827-839 (1992).
19. Johansson, R.S. & Flanagan, J.R. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat. Rev. Neurosci. 10, 345-359 (2009).
20. Johnson, K.O. The roles and functions of cutaneous mechanoreceptors. Curr. Opin. Neurobiol. 11, 455-461 (2001).
21. Johnson, K.O. & Lamb, G.D. Neural mechanisms of spatial tactile discrimination: neural patterns evoked by braille-like dot patterns in the monkey. J. Physiol. (Lond.) 310, 117-144 (1981).
22. Vega-Bermudez, F., Johnson, K.O. & Hsiao, S.S. Human tactile pattern recognition: active versus passive touch, velocity effects and patterns of confusion. J. Neurophysiol. 65, 531-546 (1991).
23. Blake, D.T., Johnson, K.O. & Hsiao, S.S. Monkey cutaneous SAI and RA responses to raised and depressed scanned patterns: effects of width, height, orientation, and a raised surround. J. Neurophysiol. 78, 2503-2517 (1997).
24. Panzeri, S., Petersen, R.S., Schultz, S.R., Lebedev, M. & Diamond, M.E. The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29, 769-777 (2001).
25. Gollisch, T. & Meister, M. Rapid neural coding in the retina with relative spike latencies. Science 319, 1108-1111 (2008).
26. Johansson, R.S. & Birznieks, I. First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat. Neurosci. 7, 170-177 (2004).
27. Vázquez, Y., Salinas, E. & Romo, R. Transformation of the neural code for tactile detection from thalamus to cortex. Proc. Natl. Acad. Sci. USA 110, E2635-E2644 (2013).
28. Schreiber, S., Fellous, J.M., Whitmer, D., Tiesinga, P. & Sejnowski, T.J. A new correlation-based measure of spike timing reliability. Neurocomputing 52-54, 925-931 (2003).
29. Fellous, J.M., Tiesinga, P.H., Thomas, P.J. & Sejnowski, T.J. Discovering spike patterns in neuronal responses. J. Neurosci. 24, 2989-3001 (2004).
30. Hyvärinen, J. & Poranen, A. Movement-sensitive and direction and orientation-selective cutaneous receptive fields in the hand area of the post-central gyrus in monkeys. J. Physiol. (Lond.) 283, 523-537 (1978).
31. Warren, S., Hamalainen, H.A. & Gardner, E.P. Objective classification of motion-and direction-sensitive neurons in primary somatosensory cortex of awake monkeys. J. Neurophysiol. 56, 598-622 (1986).
32. Pei, Y.C., Hsiao, S.S., Craig, J.C. & Bensmaia, S.J. Neural mechanisms of tactile motion integration in somatosensory cortex. Neuron 69, 536-547 (2011).
33. Khalsa, P.S., Friedman, R.M., Srinivasan, M.A. & Lamotte, R.H. Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors. J. Neurophysiol. 79, 3238-3251 (1998).
34. Phillips, J.R. & Johnson, K.O. Tactile spatial resolution. III. A continuum mechanics model of skin predicting mechanoreceptor responses to bars, edges, and gratings. J. Neurophysiol. 46, 1204-1225 (1981).
35. Goodwin, A.W. & Wheat, H.E. Sensory signals in neural populations underlying tactile perception and manipulation. Annu. Rev. Neurosci. 27, 53-77 (2004).
36. Vega-Bermudez, F. & Johnson, K.O. SA1 and RA receptive fields, response variability, and population responses mapped with a probe array. J. Neurophysiol. 81, 2701-2710 (1999).
37. Loomis, J.M. Tactile pattern perception. Perception 10, 5-27 (1981).
38. Vega-Bermudez, F. & Johnson, K.O. Surround suppression in the responses of primate SA1 and RA mechanoreceptive afferents mapped with a probe array. J. Neurophysiol. 81, 2711-2719 (1999).
39. Eagles, J.P. & Purple, R.L. Afferent fibers with multiple encoding sites. Brain Res. 77, 187-193 (1974).
40. Lindblom, Y. & Tapper, D.N. Integration of impulse activity in a peripheral sensory unit. Exp. Neurol. 15, 63-69 (1966).
41. Branco, T. & Häusser, M. The single dendritic branch as a fundamental functional unit in the nervous system. Curr. Opin. Neurobiol. 20, 494-502 (2010).
42. Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745-4765 (1992).
43. Georgopoulos, A.P., Schwartz, A.B. & Kettner, R.E. Neuronal population coding of movement direction. Science 233, 1416-1419 (1986).
44. Birznieks, I., Jenmalm, P., Goodwin, A.W. & Johansson, R.S. Encoding of direction of fingertip forces by human tactile afferents. J. Neurosci. 21, 8222-8237 (2001).
45. Stanley, G.B. Reading and writing the neural code. Nat. Neurosci. 16, 259-263 (2013).
46. Gire, D.H. et al. Temporal processing in the olfactory system: can we see a smell? Neuron 78, 416-432 (2013).
47. Panzeri, S., Brunel, N., Logothetis, N.K. & Kayser, C. Sensory neural codes using multiplexed temporal scales. Trends Neurosci. 33, 111-120 (2010).
48. König, P., Engel, A.K. & Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130-137 (1996).
49. Usrey, W.M. The role of spike timing for thalamocortical processing. Curr. Opin. Neurobiol. 12, 411-417 (2002).
50. Vallbo, A.B. & Hagbarth, K.E. Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. Exp. Neurol. 21, 270-289 (1968).