Abstract
The vibrissal-trigeminal pathway of the rat has become an increasingly important model in neuroscience to study how sensory and motor signals are encoded, processed, and integrated in the nervous system, ultimately yielding “perception“ of an object. In this chapter, we focus specifically on the role of head and vibrissa (whisker) velocity during exploratory movements. The chapter begins by describing basic vibrissal anatomy and mechanics, and shows that different studies measure “vibrissa velocity“ under very different mechanical conditions, which will give rise to very different types of mechanoreceptor activation. It is thus critical to consider forces and bending moments at the whisker base in addition to vibrissa velocity when quantifying vibrissa-object contact during natural behavior. To illustrate this point, we summarize recent results demonstrating that whisking velocity at the time of collision with an object may influence the rat’s ability to determine the radial distance to the object as well as the horizontal angle of contact. Further, we present evidence suggesting that the rat may actively select velocities at different points in the whisking trajectory, perhaps to aid localization behavior in these two dimensions. Finally, because the whiskers are always acting in concert with the head, we describe correlations between whisking behavior and head velocity. Preliminary data suggest that the position, orientation, and velocity of the head — which moves at a very different spatial and temporal scale than the vibrissae — will have a large effect on the tactile information acquired by the vibrissal system.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Ahissar E (1998) Temporal-code to rate-code conversion by neuronal phase-locked loops. Neural Comput 10: 597–650
Ahissar E, Arieli A (2001) Figuring space by time. Neuron 32: 185–201
Arabzadeh E, Panzeri S, Diamond ME (2004) Vibrissa vibration information carried by rat barrel cortex neurons. J Neurosci 24: 6011–6020
Arabzadeh E, Panzeri S, Diamond ME (2006) Deciphering the spike train of a sensory neuron: Counts and temporal patterns in the rat vibrissa pathway. J Neurosci 26: 9216–9226
Arabzadeh E, Petersen RS, Diamond ME (2003) Encoding of vibrissa vibration by rat barrel cortex neurons: Implications for texture discrimination. J Neurosci 23: 9146–9154
Arvidsson J, Rice FL (1991) Central projections of primary sensory neurons innervating different parts of the vibrissae follicles and intervibrissal skin on the mystacial pad of the rat. J Comp Neurol 309: 1–16
Belford GR, Killackey HP (1979) Development of vibrissae representation in sub-cortical trigeminal centers of the neonatal rat. J Comp Neurol 188: 63–74
Berg RW, Kleinfeld D (2003) Rhythmic whisking by the rat: Retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89: 104–117
Bermejo R, Vyas A, Zeigler H (2002) Topography of rodent whisking. I. Two dimensional monitoring of vibrissa movements. Somatosens Mot Res 19: 341–346
Birdwell JA, Solomon JH, Thajchayapong M, Taylor M, Cheely M, Towal RB, Conradt J, Hartmann MJZ (2007) Biomechanical models for radial distance determination by rat vibrissae. J Neuro-physiol 98: 2439–2455
Brecht M, Preilowski B, Merzenich MM (1997) Functional architecture of the mystacial vibrissae. Behav Brain Res 84: 81–97
Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638–2648
Carvell GE, Simons DJ (1995) Task-and subject-related differences in sensorimotor behavior during active touch. Somatosens Mot Res 12: 1–9
Dean P (1981) Visual pathways and acuity in hooded rats. Behav Brain Res 3: 239–271
Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E (2008) ‘Where’ and ‘what’ in the vibrissa sensorimotor system. Nature Rev Neurosci 9: 601–601
Dörfl J (1982) The musculature of the mystacial vibrissae of the white mouse. J Anat 135: 147–154
Dörfl J (1985) The innervation of the mystacial region of the white mouse. A topographical study. J Anat 142: 173–184
Ebara S, Kumamoto K, Matsuura T, Mazurkiewicz JE, Rice FL (2002) 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
Gibson JM, Welker WI (1983a) Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 1. Receptive field properties and threshold distributions. Somatosens Res 1: 51–67
Gibson JM, Welker WI (1983b) Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 2. Adaptation and coding of stimulus parameters. Somatosens Res 1: 95–117
Gopal V, Hartmann MJZ (2007) Using hardware models to quantify sensory data acquisition across the rat vibrissal array. J Bioinsp Biomim 2: 135–145
Grant RA, Mitchinson B, Fox CW, Prescott TJ (2009) Active touch sensing in the rat: anticipatory and regulatory control of vibrissa movements during surface exploration. J Neurophysiol 101: 862–874
Hartmann MJ, Johnson NJ, Towal RB, Assad C (2003) Natural resonance frequencies and damping characteristics of rat vibrissae. J Neurosci 23: 6510–6519
Harvey MA, Bermejo R, Zeigler HP (2001) Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks. Somatosens Mot Res 18: 211–222
Hill, DN Bermejo R, Zeigler HP, Kleinfeld D (2008) Biomechanics of the vibrissa motor plant in rat: Rhythmic whisking consists of triphasic neuromuscular activity. J Neurosci 28: 3438–3455
Hipp J, Arabzadeh E, Zorzin, E, Conradt J, Kayser C, Diamond ME, Konig P (2006) Texture signals in vibrissa vibrations. J Neurophysiol 95: 1792–1799
Jin TE, Witzemann V, Brecht M (2004) Fiber types of the intrinsic vibrissa muscle and whisking behavior. J Neurosci 24: 3386–3393
Jones LM, Depireux DA, Simons DJ, Keller A (2004) Robust temporal coding in the trigeminal system. Science 304: 1986–1989
Kaneko M, Kanayama N, Tsuji T (1998) Active antenna for contact sensing. IEEE T Robotic Autom 14: 278–291
Keller J, Strasburger H, Cerutti DT, Sabel BA (2000) Assessing spatial vision — automated measurement of the contrast-sensitivity function in the hooded rat. J Neurosci Meth. 97: 103–110
Khatri V, Bermejo R, Brumberg JC, Keller A, Zeigler HP (2009) Whisking in air: encoding of kinematics by trigeminal ganglion neurons in awake rats. J Neurophysiol 101: 1836–1846
Killackey HP (1980) Pattern-formation in the trigeminal system of the rat. Trends Neurosci 3: 303–306
Kleinfeld D, Ahissar E, Diamond ME (2006) Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol 16: 435–444
Knutsen P, Biess A, Ahissar E (2008) Vibrissal kinematics in 3D: Tight coupling of azimuth, elevation, and torsion across different whisking modes. Neuron 59: 35–42.
Krupa D, Matell M, Brisben A, Oliveira L, Nicolelis MAL (2001) Behavioral properties of the trigeminal somatosensory system in rats performing vibrissa-dependent tactile discriminations. J Neurosci 21: 5752–5763
Leiser SC, Moxon KA (2006) Relationship between physiological response type (RA and SA) and vibrissal receptive field of neurons within the rat trigeminal ganglion. J Neurophysiol 95: 3129–3145
Leiser SC, Moxon KA (2007) Responses of trigeminal ganglion neurons during natural whisking behaviors in the awake rat. Neuron 53: 117–133
Lichtenstein SH, Carvell GE, Simons DJ (1990) Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosens Mot Res 7: 47–65
Mehta S, Whitmer D, Figueroa R, Williams B, Kleinfeld D (2007) Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol 5: e15
Mitchinson B, Martin CJ, Grant RA, Prescott TJ (2007) Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc R Soc Lond B 274: 1035–1041
Moore CI (2004) Frequency-dependent processing in the vibrissa sensory system. J Neurophysiol 91: 2390–2399
Mosconi TM, Rice FL, Song MJ (1993) Sensory innervation in the inner conical body of the vibrissal follicle-sinus complex of the rat. J Comp Neurol 328: 232–251
Neimark MA, Andermann ML, Hopfield JJ, Moore CI (2003) Vibrissa resonance as a transduction mechanism for tactile encoding. J Neurosci 23: 6499–6509
Nicolelis MAL, DeOliveira LMO, Lin RCS, Chapin JK (1996) Active tactile exploration influences the functional maturation of the somatosensory system. J Neurophysiol 75: 2192–2196
Pinto DJ, Brumberg JC, Simons DJ (2000) Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83: 1158–1166
Pinto DJ, Brumberg JC, Simons DJ, Ermentrout GB (1996) A quantitative population model of vibrissa barrels: Re-examining the Wilson-Cowan equations. J Comput Neurosci 3: 247–264
Polley DB, Rickert JL, Frostig RD (2005) Vibrissa-based discrimination of object orientation determined with a rapid training paradigm. Neurobiol Learn Mem 83: 134–142
Prusky GT, Harker KT, Douglas RM, Whishaw IQ (2002) Variation in visual acuity within pigmented, and between pigmented and albino rat strains. Behav Brain Res 136: 339–348
Prusky GT, West PWR, Douglas RM (2000) Behavioral assessment of visual acuity in mice and rats. Vision Res 40: 2201–2209
Quist BW, Hartmann MJZ. (2009) Experimental validation of a quasi-static model of vibrissa bending: Effects of taper and curvature. Soc Neurosci Ann Mtg, Program Number 174.6. Chicago, IL
Rice FL (1993) Structure, vascularization, and innervation of the mystacial pad of the rat as revealed by the lectin griffonia simplicifolia. J Comp Neurol 337: 386–399
Rice FL, Fundin BT, Arvidsson J, Aldskogius H, Johansson O (1997) Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J Comp Neurol 385: 149–184
Rice FL, Mance A, Munger BL (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle-sinus complexes. J Comp Neurol 252: 154–174
Sachdev R, Berg R, Champney G, Kleinfeld D, Ebner F (2003) Unilateral vibrissa contact: changes in amplitude but not timing of rhythmic whisking. Somatosens Mot Res 20: 163–169
Sachdev R, Sato T, Ebner F (2002) Divergent movement of adjacent vibrissae. J Neurophysiol 87: 1440–1448
Shoykhet M, Doherty D, Simons D (2000) Coding of deflection velocity and amplitude by vibrissa primary afferent neurons: implications for higher level processing. Somatosens Mot Res 17: 171–180
Silveira LCL, Heywood CA, Cowey A (1987) Contrast sensitivity and visual-acuity of the pigmented rat determined electrophysiologically. Vision Res 27: 1719–1731
Solomon JH, Hartmann MJ (2006) Sensing features with robotic vibrissae. Nature 443: 525
Stüttgen MC, Kullmann S, Schwarz C (2008) Responses of rat trigeminal ganglion neurons to longitudinal vibrissa stimulation. J Neurophysiol 100: 1879–1884
Stüttgen MC, Ruter J, Schwarz C (2006) Two psychophysical channels of vibrissa deflection in rats align with two neuronal classes of primary afferents. J Neurosci 26: 7933–7941
Szwed M, Bagdasarian K, Ahissar E (2003) Encoding of vibrissal active touch. Neuron 40: 621–630
Szwed M, Bagdasarian K, Blumenfeld B, Barak O, Derdikman D, Ahissar E (2006) Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch. J Neurophysiol 95: 791–802
Temereanca S, Simons DJ (2003) Local field potentials and the encoding of vibrissa deflections by population firing synchrony in thalamic barreloids. J Neurophysiol 89: 2137–2145
Towal RB, Hartmann, MJ (2006) Right-left asymmetries in the whisking behavior of rats anticipate head movements. J Neurosci 26: 8838–8846
Towal RB, Hartmann MJZ (2008) Variability in velocity profiles during the free-air whisking behavior of unrestrained rats. J Neurophysiol 100: 740–752
Towal RB, Hartmann MJZ (2010) Principles and Applications of Active Tactile Sensing Strategies in The Rat Vibrissal System. IEEE Sensors Conference. Kona, HI. Nov 01-04, 2010
Towal RB, Quist BW, Gopal V, Solomon JH and Hartmann MJZ (2011) The morphology of the rat vibrissal array: a model for quantifying spatiotemporal patterns of whisker-object contact. PLoS Computational Biology 7:e1001120.
Van der Loos H (1976) Barreloids in mouse somatosensory thalamus. Neurosci Lett 2: 1–6
Vaziri A, Jenks RA, Boloori AR, Stanley GB (2007) Flexible probes for characterizing surface topology: From biology to technology. Exp Mech 47: 417–425
Vincent SB (1913) The tactile hair of the white rat. J Comp Neurol 23: 1–38
Welker WI (1964) Analysis of sniffing of the albino rat. Behav 22: 223–244
Williams C, Kramer E (2010) The advantages of a tapered vibrissa. PLoS One 5: e8806. doi:10 1371/journal. pone.0 008 806
Wineski L (1983) Movements of the cranial vibris-sae in the golden hamster (Mesocricetus auratus). J Zool (Lond) 200: 261–280
Wineski LE, Donald MR, Pitts SA (1988) Morphology of the vibrissal motor system in rodents exhibiting different types of exploratory behavior. Amer Zool 28: 77A
Woolsey TA, Welker C, Schwartz RH (1975) Comparative anatomical studies of SMl face cortex with special reference to occurrence of barrels in layer 4. J Comp Neurol 164: 79–94
Zucker E, Welker WI (1969) Coding of somatic sensory input by vibrissae neurons in the rat’s trigeminal ganglion. Brain Res 12: 138–156
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer-Verlag/Wien
About this chapter
Cite this chapter
Towal, R.B., Quist, B.W., Solomon, J.H., Hartmann, M.J.Z. (2012). Active sensing: Head and vibrissal velocity during exploratory behaviors of the rat. In: Frontiers in Sensing. Springer, Vienna. https://doi.org/10.1007/978-3-211-99749-9_14
Download citation
DOI: https://doi.org/10.1007/978-3-211-99749-9_14
Publisher Name: Springer, Vienna
Print ISBN: 978-3-211-99748-2
Online ISBN: 978-3-211-99749-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)