Pre-neuronal morphological processing of object location by individual whiskers

Nature Neuroscience

Volumn 16, Issue 5, 2013, Pages 622-631

  Bagdasarian, Knarik ^a   Szwed, Marcin ^b   Knutsen, Per Magne ^c   Deutsch, Dudi ^a   Derdikman, Dori ^d   Pietr, MacIej ^a   Simony, Erez ^e   Ahissar, Ehud ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STRUCTURE; HAIR FOLLICLE; NERVE CELL; NONHUMAN; ORIENTATION; PRE NEURON; PRIORITY JOURNAL; RAT; VIBRISSA;

AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; ANESTHETICS; ANIMALS; BIOMECHANICS; BRAIN MAPPING; HAIR FOLLICLE; MALE; MECHANORECEPTORS; MOVEMENT; PHYSICAL STIMULATION; RATS; RATS, WISTAR; REPRODUCIBILITY OF RESULTS; TIME FACTORS; VIBRISSAE; VIDEO RECORDING; WAKEFULNESS;

EID: 84876906267     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3378     Document Type: Article

References (52)

1. Kleinfeld, D., Ahissar, E. & Diamond, M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435-444 (2006). (Pubitemid 44142265)
2. Diamond, M.E., von Heimendahl, M., Knutsen, P.M., Kleinfeld, D. & Ahissar, E. 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 9, 601-612 (2008). (Pubitemid 352032113)
3. Ebara, S., Kumamoto, K., Matsuura, T., Mazurkiewicz, J.E. & Rice, F.L. Similarities and differences in the innervation of mystacial vibrissal follicle-sinus complexes in the rat and cat: a confocal microscopic study. J. Comp. Neurol. 449, 103-119 (2002).
4. Hartmann, M.J., Johnson, N.J., Towal, R.B. & Assad, C. Mechanical characteristics of rat vibrissae: resonant frequencies and damping in isolated whiskers and in the awake behaving animal. J. Neurosci. 23, 6510-6519 (2003). (Pubitemid 36909877)
5. Ritt, J.T., Andermann, M.L. & Moore, C.I. Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats. Neuron 57, 599-613 (2008). (Pubitemid 351273990)
6. Wolfe, J. et al. Texture coding in the rat whisker system: slip-stick versus differential resonance. PLoS Biol. 6, e215 (2008).
7. Szwed, M., Bagdasarian, K. & Ahissar, E. Encoding of vibrissal active touch. Neuron 40, 621-630 (2003). (Pubitemid 37494709)
8. Szwed, M. et al. Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch. J. Neurophysiol. 95, 791-802 (2006). (Pubitemid 44699084)
9. Lottem, E. & Azouz, R. Dynamic translation of surface coarseness into whisker vibrations. J. Neurophysiol. 100, 2852-2865 (2008).
10. Arabzadeh, E., Zorzin, E. & Diamond, M.E. Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol. 3, e17 (2005).
11. Andermann, M.L., Ritt, J., Neimark, M.A. & Moore, C.I. Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high-frequency stimuli. Neuron 42, 451-463 (2004). (Pubitemid 38610143)
12. Knutsen, P.M. & Ahissar, E. Orthogonal coding of object location. Trends Neurosci. 32, 101-109 (2009).
13. Kleinfeld, D. & Deschênes, M. Neuronal basis for object location in the vibrissa scanning sensorimotor system. Neuron 72, 455-468 (2011).
14. Birdwell, J.A. et al. Biomechanical models for radial distance detection by rat vibrissae. J. Neurophysiol. 98, 2439-2455 (2007). (Pubitemid 47584424)
15. Quist, B.W. & Hartmann, M.J. Mechanical signals at the base of a rat vibrissa: the effect of intrinsic vibrissa curvature and implications for tactile exploration. J. Neurophysiol. 107, 2298-2312 (2012).
16. Solomon, J.H. & Hartmann, M.J. Radial distance determination in the rat vibrissal system and the effects of Weber's law. Phil. Trans. R. Soc. Lond. B 366, 3049-3057 (2011).
17. Boubenec, Y., Shulz, D.E. & Debregeas, G. Whisker encoding of mechanical events during active tactile exploration. Front. Behav. Neurosci. 6, 74 (2012).
18. Knutsen, P.M., Derdikman, D. & Ahissar, E. Tracking whisker and head movements in unrestrained behaving rodents. J. Neurophysiol. 93, 2294-2301 (2005). (Pubitemid 40404422)
19. Pearson, M.J., Mitchinson, B., Sullivan, J.C., Pipe, A.G. & Prescott, T.J. Biomimetic vibrissal sensing for robots. Phil. Trans. R. Soc. Lond. B 366, 3085-3096 (2011).
20. Prescott, T.J., Pearson, M.J., Mitchinson, B., Sullivan, J.C.W. & Pipe, A.G. Whisking with robots. IEEE Robot. Autom. Mag. 16, 42-50 (2009).
21. Towal, R.B., Quist, B.W., Gopal, V., Solomon, J.H. & Hartmann, M.J. The morphology of the rat vibrissal array: a model for quantifying spatiotemporal patterns of whisker-object contact. PLoS Comput. Biol. 7, e1001120 (2011).
22. Pfeifer, R. & Gomez, G. Morphological computation: connecting brain, body and environment. in Creating Brain-like Intelligence: From Basic Principles to Complex Intelligent Systems (eds. Sendhoff, B., Körner, E., Sporns, O., Ritter, H. & Doya, K.) 66-83 (2009).
23. Knutsen, P.M., Pietr, M. & Ahissar, E. Haptic object localization in the vibrissal system: behavior and performance. J. Neurosci. 26, 8451-8464 (2006).
24. O'Connor, D.H. et al. Vibrissa-based object localization in head-fixed mice. J. Neurosci. 30, 1947-1967 (2010).
25. Deutsch, D., Pietr, M., Knutsen, P.M., Ahissar, E. & Schneidman, E. Fast feedback in active sensing: touch-induced changes to whisker-object interaction. PLoS ONE 7, e44272 (2012).
26. Mitchinson, B., Martin, C.J., Grant, R.A. & Prescott, T.J. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc. Biol. Sci. 274, 1035-1041 (2007). (Pubitemid 47056727)
27. O'Regan, J.K. & Noe, A. A sensorimotor account of vision and visual consciousness. Behav. Brain Sci. 24, 939-973, discussion 973-1031 (2001). (Pubitemid 34965956)
28. Euler, L. Eneström Number 65: Methodus Inveniendi Lineas Curvas Maximi Minimive Proprietate Gaudentes, Sive Solutio Problematis Isoperimetrici Lattissimo Sensu Accepti (Marcum-Michaelem Bousquet and Socios, Geneva, 1744).
29. Hill, D.N., Curtis, J.C., Moore, J.D. & Kleinfeld, D. Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 72, 344-356 (2011).
30. Gordon, G. & Ahissar, E. Hierarchical curiosity loops and active sensing. Neural Netw. 32, 119-129 (2012).
31. Ahissar, E., Abeles, M., Ahissar, M., Haidarliu, S. & Vaadia, E. Hebbian-like functional plasticity in the auditory cortex of the behaving monkey. Neuropharmacology 37, 633-655 (1998). (Pubitemid 28306951)
32. Ego-Stengel, V., Shulz, D.E., Haidarliu, S., Sosnik, R. & Ahissar, E. Acetylcholine-dependent induction and expression of functional plasticity in the barrel cortex of the adult rat. J. Neurophysiol. 86, 422-437 (2001). (Pubitemid 32623246)
33. Bahar, A., Dudai, Y. & Ahissar, E. Neural signature of taste familiarity in the gustatory cortex of the freely behaving rat. J. Neurophysiol. 92, 3298-3308 (2004). (Pubitemid 39506308)
34. Saig, A., Gordon, G., Assa, E., Arieli, A. & Ahissar, E. Motor-sensory confluence in tactile perception. J. Neurosci. 32, 14022-14032 (2012).
35. Ahissar, E. & Knutsen, P.M. Object localization with whiskers. Biol. Cybern. 98, 449-458 (2008). (Pubitemid 351706394)
36. Horev, G. et al. Motor-sensory convergence in object localization: a comparative study in rats and humans. Phil. Trans. R. Soc. Lond. B 366, 3070-3076 (2011).
37. Mitchinson, B. et al. Empirically inspired simulated electro-mechanical model of the rat mystacial follicle-sinus complex. Proc. Biol. Sci. 271, 2509-2516 (2004).
38. Lottem, E. & Azouz, R. A unifying framework underlying mechanotransduction in the somatosensory system. J. Neurosci. 31, 8520-8532 (2011).
39. Hill, D.N., Bermejo, R., Zeigler, H.P. & Kleinfeld, D. Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity. J. Neurosci. 28, 3438-3455 (2008). (Pubitemid 351469326)
40. Simony, E. et al. Temporal and spatial characteristics of vibrissa responses to motor commands. J. Neurosci. 30, 8935-8952 (2010).
41. Haidarliu, S., Simony, E., Golomb, D. & Ahissar, E. Muscle architecture in the mystacial pad of the rat. Anat. Rec. (Hoboken) 293, 1192-1206 (2010).
42. Stüttgen, M.C., Kullmann, S. & Schwarz, C. Responses of rat trigeminal ganglion neurons to longitudinal whisker stimulation. J. Neurophysiol. 100, 1879-1884 (2008).
43. Pammer, L. et al. The mechanical variables underlying object localization along the axis of the whisker. J. Neurosci. (in the press) (2013).
44. O'Connor, D.H., Peron, S.P., Huber, D. & Svoboda, K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67, 1048-1061 (2010).
45. Knutsen, P.M., Biess, A. & Ahissar, E. Vibrissal kinematics in 3D: tight coupling of azimuth, elevation, and torsion across different whisking modes. Neuron 59, 35-42 (2008). (Pubitemid 351905853)
46. Sachdev, R.N., Sato, T. & Ebner, F.F. Divergent movement of adjacent whiskers. J. Neurophysiol. 87, 1440-1448 (2002). (Pubitemid 34670811)
47. Chiel, H.J., Ting, L.H., Ekeberg, Ö. & Hartmann, M.J.Z. The brain in its body: motor control and sensing in a biomechanical context. J. Neurosci. 29, 12807-12814 (2009).
48. Cramer, N.P. & Keller, A. Cortical control of a whisking central pattern generator. J. Neurophysiol. 96, 209-217 (2006). (Pubitemid 44015354)
49. Harish, O. & Golomb, D. Control of the firing patterns of vibrissa motoneurons by modulatory and phasic synaptic inputs: a modeling study. J. Neurophysiol. 103, 2684-2699 (2010).
50. Herfst, L.J. & Brecht, M. Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat. J. Neurophysiol. 99, 2821-2832 (2008).
51. Pietr, M.D., Knutsen, P.M., Shore, D.I., Ahissar, E. & Vogel, Z. Cannabinoids reveal separate controls for whisking amplitude and timing in rats. J. Neurophysiol. 104, 2532-2542 (2010).
52. Weisstein, J.S., Goldsby, R.E. & O'Donnell, R.J. Oncologic approaches to pediatric limb preservation. J. Am. Acad. Orthop. Surg. 13, 544-554 (2005).