Skip to main content
Log in

Sensing the effect of body load in legs: responses of tibial campaniform sensilla to forces applied to the thorax in freely standing cockroaches

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Sense organs in the legs that detect body weight are an important component in the regulation of posture and locomotion. We tested the abilities of tibial campaniform sensilla, receptors that can monitor forces in the cockroach leg, to encode variations in body load in freely standing animals. Small magnets were attached to the thorax and currents were applied to a coil below the substrate. Sensory and motor activities were monitored neurographically. The tibial sensilla could show vigorous discharges to changing forces when animals stood upon their legs and actively supported the body weight. Firing of individual afferents depended upon the orientation of the receptor’s cuticular cap: proximal sensilla (oriented perpendicular to the leg axis) discharged to force increases while distal receptors (parallel to the leg) fired to decreasing forces. Proximal sensillum discharges were prolonged and could encode the level of load when increases were sustained. Firing of the trochanteral extensor motoneuron was also strongly modulated by changing load. In some postures, sensillum discharges paralleled changes in motor frequency consistent with a known interjoint reflex. These findings demonstrate that tibial campaniform sensilla can monitor the effects of body weight upon the legs and may aid in generating support of body load.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–D
Fig. 2A–D
Fig. 3. A
Fig. 4A,B
Fig. 5A–E
Fig. 6A–E

Similar content being viewed by others

References

  • Akay T, Bässler U, Gerharz P, Büschges A (2001) The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint. J Neurophysiol 85:594–604

    CAS  PubMed  Google Scholar 

  • Alexander RM (1988) Elastic mechanisms in animal movement. Cambridge University Press, Cambridge

  • Aniss AM, Diener HC, Hore J, Gandevia SC, Burke D (1990) Behavior of human muscle receptors when reliant on proprioceptive feedback during standing. J Neurophysiol 64:661–670

    CAS  PubMed  Google Scholar 

  • Bohnenberger J (1981) Matched transfer characteristics of single units in a compound slit sense organ. J Comp Physiol 142:391–402

    Google Scholar 

  • Chang YH, Huang HW, Hamerski CM, Kram R (2000) The independent effects of gravity and inertia on running mechanics. J Exp Biol 203:229–238

    PubMed  Google Scholar 

  • Chapman KM, Smith RS (1963) A linear transfer function underlying impulse frequency modulation in a cockroach mechanoreceptor. Nature 197:699–700

    Google Scholar 

  • Cruse H, Riemenschneider D, Stammer W (1989) Control of body position of a stick insect standing on uneven surfaces. Biol Cybern 61:71–77

    Google Scholar 

  • Cruse H, Dautenhahn K, Schreiner H (1992) Coactivation of leg reflexes in the stick insect. Biol Cybern 67:369–375

    Google Scholar 

  • Cruse H, Schmitz J, Braun U, Schweins A (1993) Control of body height in a stick insect walking on a treadwheel. J Exp Biol 181:141–155

    Google Scholar 

  • Duysens J, Clarac F, Cruse H (2000) Load regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80:83–133

    CAS  PubMed  Google Scholar 

  • Eckweiler W, Seyfarth E-A (1988) Tactile hairs and the adjustment of body height in wandering spiders: behavior, leg reflexes, and afferent projections in the leg ganglia. J Comp Physiol 162:611–621

    Google Scholar 

  • French AS, Torkkeli PH (1994) The time course of sensory adaptation in the cockroach tactile spine. Neurosci Lett 178:147–150

    CAS  PubMed  Google Scholar 

  • Full RJ, Tu MS (1991) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. J Exp Biol 156:215–231

    CAS  PubMed  Google Scholar 

  • Full RJ, Blickhan R, Ting LH (1991) Leg design in hexapedal runners. J Exp Biol 158:369–90

    PubMed  Google Scholar 

  • Horak FB, Macpherson JM (1996) Postural orientation and equilibrium. In: Rowell L, Shepard J (eds) Handbook of physiology, sect 12. Integration of motor, circulatory, respiratory and metabolic control during exercise. Oxford University Press, New York, pp 255–292

  • Jacobs R, Macpherson JM (1996) Two functional muscle groupings during postural equilibrium tasks in standing cats. J Neurophysiol 76:2402–2411

    CAS  PubMed  Google Scholar 

  • Jankowska E (2001) Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol (Lond) 533:31–40

    Google Scholar 

  • Kemmerling S, Varjú D (1981) Regulation of the body-substrate-distance in the stick insect: responses to sinusoidal stimulation. Biol Cybern 39:129–137

    Google Scholar 

  • Kemmerling S, Varjú D (1982) Regulation of the body-substrate-distance in the stick insect: step responses and modeling the control system. Biol Cybern 44:59–66

    Google Scholar 

  • Kram R (1996) Inexpensive load carrying by rhinoceros beetles. J Exp Biol 199:609–611

    PubMed  Google Scholar 

  • Kram R, Full RJ (1997) Three-dimensional kinematics and limb kinetic energy of running cockroaches. J Exp Biol 200:1919–1929

    PubMed  Google Scholar 

  • Krauthamer V, Fourtner CR (1978) Locomotory activity in the extensor and flexor tibiae of the cockroach, Periplaneta americana. J Insect Physiol 24:813–819

    Article  Google Scholar 

  • Larsen GS, Frazier SF, Fish SE, Zill SN (1995) Effects of load inversion in cockroach walking. J Comp Physiol A 176:229–238

    CAS  PubMed  Google Scholar 

  • Libersat F, Clarac F, Zill SN (1987) Force-sensitive mechanoreceptors of the dactyl of the crab: single-unit responses during walking and evaluation of function. J Neurophysiol 57:1618-1637

    CAS  PubMed  Google Scholar 

  • Maloiy GM, Heglund NC, Prager LM, Cavagna GA, Taylor CR (1986) Energetic cost of carrying loads: have African women discovered an economic way? Nature 319:668–669

    CAS  PubMed  Google Scholar 

  • McIlroy WE, Maki BE (1993) Do anticipatory postural adjustments precede compensatory stepping reactions evoked by perturbation? Neurosci Lett 164:199–202

    CAS  PubMed  Google Scholar 

  • Milde JJ, Seyfarth E-A (1988) Tactile hairs and leg reflexes in wandering spiders: physiological and anatomical correlates of reflex activity in the leg ganglia. J Comp Physiol A 162:623–631

    Google Scholar 

  • Neff D, Frazier SF, Quimby L, Wang R, Zill S (2000) Identification of resilin in the leg of the cockroach: confirmation by a simple method using pH dependence of UV fluorescence. Arthropod Struct Dev 29:75–83

    Article  Google Scholar 

  • Noah JA, Quimby L, Frazier SF, Zill SN (2001) Force receptors in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered. J Comp Physiol A 187:769–784

    Article  CAS  PubMed  Google Scholar 

  • Nye SW, Ritzmann RE (1992) Motion analysis of leg joints associated with escape turns of the cockroach, Periplaneta americana. J Comp Physiol A 177:183–194

    Google Scholar 

  • Pearson KG (1972) Central programming and reflex control of walking in the cockroach. J Exp Biol 56:173–193

    Google Scholar 

  • Pratt CA (1995) Evidence of positive force feedback among hindlimb extensors in the intact standing cat. J Neurophysiol 73:2578–2583

    Google Scholar 

  • Pringle JWS (1938) Proprioception in insects. II. The action of the campaniform sensilla on the legs. J Exp Biol 15:114–131

    Google Scholar 

  • Prochazka A (1996) Proprioceptive feedback and equilibrium. In: Rowell L, Shepard J (eds) Handbook of physiology, sect 12. Oxford University Press, New York, pp 89–128

  • Prochazka A, Westerman RA, Ziccone SP (1977) Ia afferent activity during a variety of voluntary movements in the cat. J Physiol (Lond) 268:423–448

    Google Scholar 

  • Puniello MS, McGibbon CA, Krebs DE (2000) Lifting characteristics of functionally limited elders. J Rehabil Res Dev 37:341–352

    CAS  PubMed  Google Scholar 

  • Ridgel AL, Frazier SF, DiCaprio RA, Zill SN (1999) Active signaling of leg loading and unloading in the cockroach. J Neurophysiol 81:1432–1437

    CAS  PubMed  Google Scholar 

  • Ridgel AL, Frazier SF, DiCaprio RA, Zill SN (2000) Encoding of forces by cockroach tibial campaniform sensilla: implications in dynamic control of posture and locomotion. J Comp Physiol A 186:359–374

    Article  CAS  PubMed  Google Scholar 

  • Ridgel AL, Frazier SF, Zill SN (2001) Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches. J Comp Physiol A 187:405–420

    PubMed  Google Scholar 

  • Schmitz J (1986a) The depressor trochanteris motoneurons and their role in the coxo-trochanteral feedback loop in the stick insect Carausius morosus. Biol Cybern 55:25–34

    Google Scholar 

  • Schmitz J (1986b) Properties of the feedback system controlling the coxa-trochanter joint in the stick insect Carausius morosus. Biol Cybern 55:35–42

    Google Scholar 

  • Schmitz J, Stein W (2000) Convergence of load and movement information onto leg motoneurons in insects. J Neurobiol 42:424–436

    Article  CAS  PubMed  Google Scholar 

  • Smith JL, Carlson-Kuhta P (1995) Unexpected motor patterns for hindlimb muscles during slope walking in the cat. J Neurophysiol 74:2211–5

    CAS  PubMed  Google Scholar 

  • Spinola SM, Chapman KM (1975) Proprioceptive indentation of the campaniform sensilla of cockroach legs. J Comp Physiol 96:257–272

    Google Scholar 

  • Stein W, Schmitz J (1999) Multimodal convergence of presynaptic afferent inhibition in insect proprioceptors. J Neurophysiol 82:512–514

    CAS  PubMed  Google Scholar 

  • Tryba AK, Ritzmann RE (2000) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. J Neurophysiol 83:3323–3336

    PubMed  Google Scholar 

  • Watson JT, Ritzmann RE (1998) Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis. I. Slow running. J Comp Physiol A 182:11–22

    Article  PubMed  Google Scholar 

  • Wendler G (1966) The co-ordination of walking movements in arthropods. In: Nervous and hormonal mechanisms of integration. Symp Soc Exp Biol 20:229–249

    Google Scholar 

  • Zill SN (1987) Selective mechanical stimulation of an identified proprioceptor in freely moving locusts: role of resistance reflexes in active posture. Brain Res 417:195-198

    Article  CAS  PubMed  Google Scholar 

  • Zill SN (1990) Mechanoreceptors and proprioceptors. In: Huber I, Masler, EP, Rao BR (eds) Cockroaches as models for neurobiology, vol II: applications in biomedical research. CRC Press, Boca Raton, Florida, pp 247- 267

  • Zill SN (1993) Load compensatory reactions in insects: swaying and stepping strategies in posture and locomotion. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, San Diego, pp 43–68

  • Zill SN, Frazier SF (1990) Responses of locusts in a paradigm which tests postural load compensatory reactions. Brain Res 535:1–8

    CAS  PubMed  Google Scholar 

  • Zill SN, Jepson-Innes KA (1988) Evolutionary adaptation of a reflex system: sensory hysteresis counters muscle ‘catch’ tension. J Comp Physiol A 164:43-48

    CAS  PubMed  Google Scholar 

  • Zill SN, Moran DT (1981a) The exoskeleton and insect proprioception. I. Responses of tibial campaniform sensilla to external and muscle generated forces in the American cockroach, Periplaneta americana. J Exp Biol 91:1–24

    Google Scholar 

  • Zill SN, Moran DT (1981b) The exoskeleton and insect proprioception. III. Activity of tibial campaniform sensilla during walking in the American cockroach, Periplaneta americana. J Exp Biol 94:57–75

    Google Scholar 

  • Zill SN, Frazier SF, Lankenau J, Jepson-Innes KA (1992) Characteristics of dynamic postural reactions in the locust hindleg. J Comp Physiol A 170:761–772

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors warmly thank Josef Schmitz, Fred Delcomyn and Holk Cruse for their helpful comments on the manuscript. This work was supported by NSF grant IBN-0235997 and Office of Naval Research URISP Grant N00014-96-1-0694.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. N. Zill.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Noah, J.A., Quimby, L., Frazier, S.F. et al. Sensing the effect of body load in legs: responses of tibial campaniform sensilla to forces applied to the thorax in freely standing cockroaches. J Comp Physiol A 190, 201–215 (2004). https://doi.org/10.1007/s00359-003-0487-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-003-0487-y

Keywords