Skip to main content

Matched Filtering in Active Whisker Touch

Abstract

Whiskers are present on most mammals, and whisker specialists, such as rodents, pinnipeds and insectivores, can actively position their whiskers to efficiently guide navigation, locomotion and exploration. That only a small number of whiskers give enough information about the local environment to be the primary tactile sense in many mammals has prompted researchers to explore how well adapted the whisker system is and how “matched” these sensors are to their function. In this chapter, we suggest that whisker touch systems have a matched filter design by arguing that (i) the layout of the vibrissae and their mechanical properties provide a computationally cheap way to gather tactile and spatial information; (ii) this layout is topographically mapped throughout the brain, enabling temporal and spatial information to be preserved easily during processing, freeing up other areas of the brain; and (iii) movement of the whiskers can focus the sensors onto salient regions of space and also control the amount, type and quality of information gathered from an environment. That anatomical and behavioural characteristics are maintained throughout many different mammalian orders indicates the importance of vibrissal touch sensing in arboreal, nocturnal animals, hence its conservation throughout mammalian evolution.

Keywords

  • Superior Colliculus
  • Central Pattern Generator
  • Intrinsic Muscle
  • Active Touch
  • Extrinsic Muscle

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-319-25492-0_3
  • Chapter length: 24 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   109.00
Price excludes VAT (USA)
  • ISBN: 978-3-319-25492-0
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   139.99
Price excludes VAT (USA)
Hardcover Book
USD   199.99
Price excludes VAT (USA)
Fig. 3.1
Fig. 3.2
Fig. 3.3
Fig. 3.4
Fig. 3.5
Fig. 3.6

References

  • Ahl AS (1986) The role of vibrissae in behavior – a status review. Vet Res Commun 10:245–268

    CAS  CrossRef  Google Scholar 

  • Anjum F, Turni H, Mulder PG, van der Burg J, Brecht M (2006) Tactile guidance of prey capture in Etruscan shrews. Proc Natl Acad Sci U S A 103:16544–16549

    CAS  CrossRef  Google Scholar 

  • Arkley K, Grant RA, Mitchinson B, Prescott TJ (2014) Strategy change in vibrissal active sensing during rat locomotion. Curr Biol 24(13):1507–1512

    CAS  CrossRef  Google Scholar 

  • Barnett SA (2007) The rat: a study in behaviour. Aldine Transaction, London

    Google Scholar 

  • Baumann KI, Chan E, Halata Z, Senok SS, Yung WH (1996) An isolated rat vibrissal preparation with stable responses of slowly adapting mechanoreceptors. Neurosci Lett 213:1–4

    CAS  CrossRef  Google Scholar 

  • Benedetti F (1991) The postnatal emergence of a functional somatosensory representation in the superior colliculus of the mouse. Dev Brain Res 60(1):51–57

    CAS  CrossRef  Google Scholar 

  • Berg RW, Kleinfeld D (2003a) Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89:104–117

    CrossRef  Google Scholar 

  • Berg RW, Kleinfeld D (2003b) Vibrissa movement elicited by rhythmic electrical microstimulation to motor cortex in the aroused rat mimics exploratory whisking. J Neurophysiol 90:2950–2963

    CrossRef  Google Scholar 

  • Birdwell JA, Solomon JH, Thajchayapong M, Taylor MA, Cheely M, Towal RB, Conradt J, Hartmann MJZ (2007) Biomechanical models for radial distance determination by the rat vibrissal system. J Neurophysiol 98:2439–2455

    CrossRef  Google Scholar 

  • Brecht M, Preilowski B, Merzenich MM (1997) Functional architecture of the mystacial vibrissae. Behav Brain Res 84(1–2):81–97

    CAS  CrossRef  Google Scholar 

  • Bugbee NM, Eichelman BS (1972) Sensory alterations and aggressive behaviour in the rat. Physiol Behav 8:981–985

    CAS  CrossRef  Google Scholar 

  • Cao Y, Roy S, Sachdev RN, Heck DH (2012) Dynamic correlation between whisking and breathing rhythms in mice. J Neurosci 32:1653–1659

    CAS  CrossRef  Google Scholar 

  • Carlson AJ, Hoelzel F (1949) Influence of texture of food on its acceptance by rats. Science 109:63–64

    CAS  CrossRef  Google Scholar 

  • Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10(8):2638–2648

    CAS  Google Scholar 

  • Christie D, Terry P, Oakley DA (1990) The effect of unilateral anteromedial cortex lesions on prey-catching and spatio-motor behaviour in the rat. Behav Brain Res 37:263–268

    CAS  CrossRef  Google Scholar 

  • Cramer NP, Keller A (2006) Cortical control of a whisking central pattern generator. J Neurophysiol 96:209–217

    CrossRef  Google Scholar 

  • Cramer N, Li Y, Keller A (2007) The whisking rhythm generator: a novel mammalian network for the generation of movement. J Neurophysiol 97(3):2148–2158

    CAS  CrossRef  Google Scholar 

  • Czech-Damal NU, Liebschner A, Miersch L, Klauer G, Hanke FD, Marshall C, Dehnhardt G, Hanke W (2011) Electroreception in the Guiana dolphin (Sotalia guianensis). Proc R Soc B 279(1729):663–668

    CrossRef  Google Scholar 

  • Dehnhardt G (1994) Tactile size discrimination by a California sea lion (Zalophus californianus) using its mystacial vibrissae. J Comp Physiol A 175:791–800

    CAS  CrossRef  Google Scholar 

  • Dehnhardt G, Dücker G (1996) Tactual discrimination of size and shape by a California sea lion (Zalophus californianus). Anim Learn Behav 24(4):366–374

    CrossRef  Google Scholar 

  • Dehnhardt G, Kaminski A (1995) Sensitivity of the mystacial vibrissae of harbor seals (phoca- vitulina) for size differences of actively touched objects. J Exp Biol 198:2317

    CAS  Google Scholar 

  • Dehnhardt G, Mauck B, Bleckmann H (1998) Seal whiskers detect water movements. Nature 394(6690):235–236

    CAS  CrossRef  Google Scholar 

  • Dehnhardt G, Mauck B (2008) Mechanoreception in secondarily aquatic vertebrates. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold–adaptations in secondarily aquatic vertebrates. University of California Press, Berkely, pp 295–314

    Google Scholar 

  • Dehnhardt G, Mauck B, Hanke W, Bleckmann H (2001) Hydrodynamic trail-following in harbor seals (Phoca vitulina). Science 293:102–104

    CAS  CrossRef  Google Scholar 

  • Deschenes M, Timofeeva E, Lavallee P (2003) The relay of high-frequency sensory signals in the Whisker-to-barreloid pathway. J Neurosci 23:6778–6787

    CAS  Google Scholar 

  • Deschênes M, Moore J, Kleinfeld D (2012) Sniffing and whisking in rodents. Curr Opin Neurobiol 22(2):243–250

    CrossRef  Google Scholar 

  • Diamond ME, Petersen RS, Harris JA, Panzeri S (2003) Investigations into the organization of information in sensory cortex. J Physiol Paris 97:529–536

    CrossRef  Google Scholar 

  • Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E (2008) ‘Where’ and ‘what’ in the whisker sensorimotor system. Nat Rev Neurosci 9:601–612

    CAS  CrossRef  Google Scholar 

  • Dorfl J (1982) The musculature of the mystacial vibrissae of the white-mouse. J Anat 135:147–154

    CAS  Google Scholar 

  • Dräger UC, Hubel DH (1976) Topography of visual and somatosensory projections to mouse superior colliculus. J Neurophysiol 39(1):91–101

    Google Scholar 

  • Dyck RH (2005) Vibrissae. In: Wishaw IQ, Kolb B (eds) The behavior of the laboratory rat: a handbook with tests. Oxford University Press, Oxford, pp 81–89

    Google Scholar 

  • Feldman DE, Brecht M (2005) Map plasticity in somatosensory cortex. Science 310(5749):81

    CrossRef  Google Scholar 

  • Friedman WA, Jones LM, Cramer NP, Kwegyir-Afful EE, Zeigler HP, Keller A (2006). Anticipatory activity of motor cortex in relation to rhythmic whisking. J Neurophysiol, 95(2):1274–1277

    Google Scholar 

  • Gao P, Bermejo R, Zeigler HP (2001) Whisker deafferentation and rodent whisking patterns: behavioral evidence for a central pattern generator. J Neurosci 21:5374–5380

    CAS  Google Scholar 

  • Glaser N, Wieskotten S, Otter C, Dehnhardt G, Hanke W (2011) Hydrodynamic trial following in a California sea lion (Zalophus Californianus). J Comp Physiol A 197:141–151

    CrossRef  Google Scholar 

  • Grant R, Mitchinson B, Fox C, Prescott TJ (2009) Active touch sensing in the rat: anticipatory and regulatory control of whisker movements during surface exploration. J Neurophysiol 101:862–874

    CrossRef  Google Scholar 

  • Grant RA, Sperber A, Prescott TJ (2012) The role of orienting in vibrissal touch sensing. Front Behav Neurosci 6:39

    CrossRef  Google Scholar 

  • Grant RA, Weiskotten S, Wengst N, Prescott TJ, Dehnhardt G (2013a) Vibrissal touch sensing in the harbour seal (Phoca vitulina): how do seals judge size? J Comp Physiol A 199(6):521–533, In Special Issue on the Sensory Biology of Aquatic Mammals

    CrossRef  Google Scholar 

  • Grant RA, Haidarliu S, Kennerley NJ, Prescott TJ (2013b) The evolution of active vibrissal sensing in mammals: evidence from vibrissal musculature and function in the marsupial opossum Monodelphis domestica. J Exp Biol 216(18):3483–3494

    CrossRef  Google Scholar 

  • Grant RA, Sharp PS, Kennerley AJ, Berwick J, Grierson A, Ramesh T, Prescott TJ (2013c) Abnormalities in whisking behaviour are associated with lesions in brain stem nuclei in a mouse model of amyotrophic lateral sclerosis. Behav Brain Res 259:274–283

    CrossRef  Google Scholar 

  • Grant R, Itskov PM, Towal B, Prescott TJ (eds) (2014) Active touch sensing. Frontiers E-books

    Google Scholar 

  • Gustafson JW, Felbain-Keramidas SL (1977) Behavioral and neural approaches to the function of the mystacial vibrissae. Psychol Bull 84:477–488

    CAS  CrossRef  Google Scholar 

  • Haidarliu S, Ahissar E (1997) Spatial organization of facial vibrissae and cortical barrels in the guinea pig and golden hamster. J Comp Neurol 385:515–527

    CAS  CrossRef  Google Scholar 

  • Haidarliu S, Ahissar E (2001) Size gradients in the barreloids in the rat thalamus. J Comp Neurol 429:372–387

    CAS  CrossRef  Google Scholar 

  • Haidarliu S, Simony E, Golomb D, Ahissar E (2010) Muscle architecture in the mystacial pad of the rat. Anat Rec 293:1192–1206

    CrossRef  Google Scholar 

  • Hanke W, Witte M, Miersch L, Brede M, Oeffner J, Michael M, Hanke F, Leder A, Dehnhardt G (2010) Harbor seal vibrissa morphology suppresses vortex-induced vibrations. J Exp Boil 213:2665–2672

    CrossRef  Google Scholar 

  • 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

    CAS  CrossRef  Google Scholar 

  • Hemelt ME, Keller A (2007) Superior sensation: superior colliculus participation in rat vibrissa system. BMC Neurosci 8(1):12

    CrossRef  Google Scholar 

  • Hyvärinen H (1989) Diving in darkness: whiskers as sense organs of the Ringed seal (Phoca hispida). J Zool 238:663–678 system. BMC Neurosci 8:12

    CrossRef  Google Scholar 

  • Ibrahim L, Wright EA (1975) The growth of rats and mice vibrissae under normal and some abnormal conditions. J Embryol Exp Morphol 33:831–844

    CAS  Google Scholar 

  • Ivanco TL, Pellis SM, Whishaw IQ (1996) Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems. Behav Brain Res 79:163–181

    CAS  CrossRef  Google Scholar 

  • Jenkinson EW, Glickstein M (2000) Whiskers, barrels, and cortical efferent pathways in gap crossing by rats. J Neurophysiol 84:1781–1789

    CAS  Google Scholar 

  • Ji Q, Luo Z-X, Yuan C-X, Wible JR, Zhang J-P, Georgi JA (2002) The earliest known eutherian mammal. Nature 416:816–822

    CAS  CrossRef  Google Scholar 

  • Johansson RS, Vallbo AB (1979) Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 286:283–300

    CAS  CrossRef  Google Scholar 

  • Knutsen PM, Biess A, Ahissar E (2008) Vibrissal kinematics in 3D: tight coupling of azimuth, elevation, and torsion across different whisking modes. Neuron 59:35–42

    CAS  CrossRef  Google Scholar 

  • Krupa DJ, Brisben AJ, Nicolelis MA (2001) A multi-channel whisker stimulator for producing spatiotemporally complex tactile stimuli. J Neurosci Methods 104:199–208

    CAS  CrossRef  Google Scholar 

  • Luo Z-X, Yuan C-X, Meng Q-J, Ji Q (2011) A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476:442–445

    CAS  CrossRef  Google Scholar 

  • Lyne AG (1959) The systematic and adaptive significance of the vibrissae in the Marsupialia. Proc Zool Soc Lond 133:79–133

    CrossRef  Google Scholar 

  • Maderson PFA (1972) When? Why? And how? Some speculations on the evolution of the vertebrate integument. Am Zool 12:159–171

    CrossRef  Google Scholar 

  • Maderson PFA (2003) Mammalian skin evolution: a re-evaluation. Exp Dermatol 12:233–236

    CAS  CrossRef  Google Scholar 

  • Mauck B, Eysel U, Dehnhardt G (2000) Selective heating of vibrissal follicles in seals (Phoca vitulina) and dolphins (Sotalia fluviatilis guianensis). J Exp Biol 203(14):2125–2131

    CAS  Google Scholar 

  • Milne AO, Grant RA (2014) Characterisation of whisker control in the California sea lion (Zalophus californianus) during a complex, dynamic sensorimotor task. J Comp Physiol A 200(10):871–879

    CrossRef  Google Scholar 

  • Mitchinson B, Prescott TJ (2013) Whisker movements reveal spatial attention: a unified computational model of active sensing control in the rat. PLoS Comput Biol 9(9):e1003236

    CAS  CrossRef  Google Scholar 

  • Mitchinson B, Gurney KN, Redgrave P, Melhuish C, Pipe AG, Pearson M, Gilhespy I, Prescott TJ (2004) Empirically inspired simulated electro-mechanical model of the rat mystacial follicle-sinus complex. Proc Biol Sci 271:2509–2516

    CrossRef  Google Scholar 

  • Mitchinson B, Martin CJ, Grant RA, Prescott TJ (2007) Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc Biol Sci 274:1035–1041

    CrossRef  Google Scholar 

  • Mitchinson B, Grant RA, Arkley KP, Perkon I, Prescott TJ (2011) Active vibrissal sensing in rodents and marsupials. Phil Trans B 366(1581):3037–3048

    CrossRef  Google Scholar 

  • Moore CI, Andermann ML (2005) The vibrissa resonance hypothesis. In: Somatosensory plasticity, Ebner FF (ed) CRC Press, Taylor & Francis, London, pp 21–60

    Google Scholar 

  • Moore JD, Deschenes M, Furata T, Huber D, Smear MC, Demers M, Kleinfeld D (2013) Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature 497:205–210

    CAS  CrossRef  Google Scholar 

  • Muchlinski MN, Durham EL, Smith TD, Burrows AM (2013) Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and “face touch”. Am J Phys Anthropol 150(2):301–312

    CrossRef  Google Scholar 

  • Pocock RI (1914) On the facial vibrissae of mammalia. Proc Zool Soc Lond 84:889–912

    CrossRef  Google Scholar 

  • Prescott TJ, Diamond ME, Wing AM (2011) Active touch sensing. Phil Trans R Soc Lond B: Biol Sci 366(1581):2989–2995

    CrossRef  Google Scholar 

  • Reep RL, Stoll ML, Marshall CD, Homer BL, Samuelson DA (2001) Microanatomy of facial vibrissae in the Florida manatee: the basis for specialized sensory function and oripulation. Brain Behav Evol 58:1–14

    CAS  CrossRef  Google Scholar 

  • Rice FL, Mance A, Munger BL (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of the vibrissal follicle-sinus complexes. J Comp Neurol 252:154–174

    CAS  CrossRef  Google Scholar 

  • Rowe TB, Macrini TE, Luo Z-X (2011) Fossil evidence on origin of the mammalian brain. Science 332(6032):955–957

    CAS  CrossRef  Google Scholar 

  • Sachdev RN, Sellien H, Ebner F (2001) Temporal organization of multi-whisker contact in rats. Somatosens Mot Res 18:91–100

    CAS  CrossRef  Google Scholar 

  • Sachdev RNS, Sato T, Ebner FF (2002) Divergent movement of adjacent whiskers. J Neurophysiol 87:1440–1448

    Google Scholar 

  • Sawyer EK, Liao CC, Qi HX, Balaram P, Matrov D, Kaas JH (2015) Subcortical barrelette-like and barreloid-like structures in the prosimian galago (Otolemur garnetti). Proc Natl Acad Sci 112(22):7079–7084

    CAS  CrossRef  Google Scholar 

  • Shuler MG, Krupa DJ, Nicolelis MA (2001) Integration of bilateral whisker stimuli in rats: role of the whisker barrel cortices. Cereb Cortex 12:86–97

    CrossRef  Google Scholar 

  • 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

    CrossRef  Google Scholar 

  • Towal RB, Hartmann MJ (2006) Right-left asymmetries in the whisking behavior of rats anticipate head movements. J Neurosci 26:8838–8846

    CAS  CrossRef  Google Scholar 

  • Vincent SB (1912) The function of the vibrissae in the behaviour of the white rat. Behav Monogr 1:1–82

    Google Scholar 

  • Vincent SB (1913) The tactile hair of the white rat. J Comp Neurol 23:1–36

    CrossRef  Google Scholar 

  • Waite PME, Tracey DJ (1995) Trigeminal sensory system. In: Paxinos G (ed) The rat nervous system. Academic, Sydney, pp 705–724

    Google Scholar 

  • Wallace DJ, Greenberg DS, Sawinski J, Rulla S, Notaro G, Kerr JND (2013) Rats maintain an overhead binocular field at the expense of constant fusion. Nature 498:65–69

    CAS  CrossRef  Google Scholar 

  • Wehner R (1987) ‘Matched filters’ – neural models of the external world. J Comp Physiol A 161:511–531

    CrossRef  Google Scholar 

  • Welker WI (1964) Analysis of sniffing in the albino rat. Behavior 22:223–224

    CrossRef  Google Scholar 

  • Wieskotten S, Dehnhardt G, Mauck B, Miersch L, Hanke W (2010a) Hydrodynamic determination of the moving direction of an artificial fin by a harbor seal (Phoca vitulina). J Exp Biol 213:2194–2200

    CAS  CrossRef  Google Scholar 

  • Wieskotten S, Dehnhardt G, Mauck B, Miersch L, Hanke W (2010b) The impact of glide phases on the trackability of hydrodynamic trials in harbor seals (Phoca vitulina). J Exp Biol 213:3734–3740

    CAS  CrossRef  Google Scholar 

  • Wolfe J, Mende C, Brecht M (2011) Social facial touch in rats. Behav Neurosci 125(6):900

    CrossRef  Google Scholar 

  • Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of the mouse cerebral cortex: the description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205–242

    CAS  CrossRef  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robyn A. Grant .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Grant, R.A., Arkley, K.P. (2016). Matched Filtering in Active Whisker Touch. In: von der Emde, G., Warrant, E. (eds) The Ecology of Animal Senses. Springer, Cham. https://doi.org/10.1007/978-3-319-25492-0_3

Download citation