Skip to main content
SpringerLink
Log in

The role of afferent activity in behavioral and neuronal plasticity in an insect

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

Summary

Cockroaches (Periplaneta americana) have been shown to adapt behaviorally, in about 1 month, to ablation of one cercus. Additionally, those giant interneurons (GIs) that normally receive their major input from the lesioned cercus become more responsive to stimulation of the intact side (Vardi and Camhi 1982 a, b). To investigate the role of afferent activity in the behavioral and neuronal plasticity, we silenced wind-evoked activity in the intact cercus by immobilizing the sensory hairs. This was carried out during the last nymphal stage which lasts for about one month. The animals were tested behaviorally and physiologically after they had molted to adults and a fresh set of mobile hairs had appeared. These animals showed no behavioral correction (Fig. 3). The responses of the GIs on the ablated side were somewhat enhanced, but they were also significantly smaller than those in animals with long-term cercal ablations and no sensory deprivation (Fig. 5). A variety of controls (Figs. 8, 9, and 10) were used to show that sensory deprivation by itself did not decrease the responsiveness of the afferents or the GIs. Thus elimination of wind-evoked activity specifically decreasesenhancement of the responses in the GIs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

GI :

giant interneuron

References

  • Brown MC, Holland RL, Hopkins WG (1981) Motor nerve sprouting. Annu Rev Neurosci 4:17–42

    Google Scholar 

  • Buño W Jr, Monti-Bloch L, Crispino L (1981a) Dynamic properties of cockroach cercal bristlelike hair sensilla. J Neurobiol 12:101–121

    Google Scholar 

  • Buño W Jr, Monti-Bloch L, Mateos A, Handler P (1981 b) Dynamic properties of cockroach cercal threadlike hair sensilla. J Neurobiol 12:123–141

    Google Scholar 

  • Callec J-J, Sattelle DB (1973) A simple technique for monitoring the synaptic actions of pharmacological agents. J Exp Biol 59:725–738

    Google Scholar 

  • Camhi JM (1976) Non-rhythmic sensory inputs: influence on locomotory outputs in arthropods. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds). Neural control of locomotion Plenum, New York, pp 561–586

    Google Scholar 

  • Camhi JM, Comer (1986) Modeling the information in groups of identified cells: giant interneurons and cockroach escape behavior. Soc Neurosci Abstr 12:202

    Google Scholar 

  • Camhi JM, Tom W (1978) The escape behavior of the cockroachPeriplaneta americana. I. Turning response to wind puffs. J Comp Physiol 128:193–201

    Google Scholar 

  • Comer C (1985) Analyzing cockroach escape behavior with lesion of individual giant interneurons. Brain Res 335:342–346

    Google Scholar 

  • Dagan D, Camhi JM (1979) Responses to wind recorded for the cereal nerve of the cockroachPeriplaneta americana. II. Directional selectivity of the sensory neurons innervating single columns of filiform hairs. J Comp Physiol 133:103–110

    Google Scholar 

  • Daley DL, Vardi N, Appignani B, Camhi JM (1981) Morphology of the giant interneurons and cereal nerve projections of the American cockroach. J Comp Neurol 196:41–52

    Google Scholar 

  • Dichgans J, Bizzi E, Morasso P, Tagliasco V (1973) Mechanism underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys. Exp Brain Res 18:548–562

    Google Scholar 

  • Dieringer N, Precht W (1979) Mechanisms of compensation for vestibular deficits in the frog. I. Modification of the excitatory commissural system. Exp Brain Res 36:312–328

    Google Scholar 

  • Dowd JP, Comer CM (1986) Testing models of sensorimotor integration: Computer simulations of escape turning behavior in the cockroach. Soc Neurosci Abstr 12:202

    Google Scholar 

  • Dyson SE, Jones DG (1984) Synaptic remodelling during development and maturation: junction differentiation and splitting as a mechansim for modifying connectivity. Dev Brain Res 13:125–137

    Google Scholar 

  • Fifkova E, Harreveld A van (1977) Long-lasting morphological changes in dendritic spines of the dentate granular cells following stimulation of the entorhinal area. J Neurocytol 6:211–230

    Google Scholar 

  • Flohr H, Bienhold H, Abeln W, Macskovics I (1981) Concepts of vestibular compensation. In: Flohr H, Precht W (eds) Lesion induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg New York, pp 153–172

    Google Scholar 

  • Harris WA (1981) Neural activity and development. Annu Rev Physiol 43:689–710

    Google Scholar 

  • Huber F (1987) Plasticity in the auditory system of crickets: phonotaxis with one ear and neuronal reorganization within the auditory pathway. J Comp Physiol 161:583–604

    Google Scholar 

  • Knudsen EI (1983) Early auditory experience aligns the auditory map of space in the optic tectum of the barn owl. Science 222:939–942

    Google Scholar 

  • Knudsen EI, Knudsen PF (1985) Vision guides the adjustment of auditory localization in young barn owls. Science 230:545–548

    Google Scholar 

  • Knudsen EI, Knudsen PF, Esterley SD (1984) Monaural occlusion alters sound localization during a sensitive period in the barn owl. J Neurosci 4:1001–1011

    Google Scholar 

  • Krasne FB (1987) Silencing normal input permits regenerating foreign afferents to innervate an identified crayfish sensory interneuron. J Neurobiol 18:61–73

    Google Scholar 

  • Maehlen J, Nja A (1982) Effects of electrical stimulation on sprouting after partial denervation of guinea-pig sympathetic ganglion cells. J Physiol (Lond) 322:151–166

    Google Scholar 

  • Matsumoto SG, Murphey RK (1977) Sensory deprivation during development decreases the responsiveness of cricket giant interneurones. J Physiol (Lond) 268:533–548

    Google Scholar 

  • Matsumoto SG, Murphey RK (1978) Sensory deprivation in the cricket nervous system: Evidence for a critical period. J Physiol (Lond) 285:159–170

    Google Scholar 

  • Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Google Scholar 

  • Murphey RK, Levine R (1980) Mechanism responsible for changes observed in response properties of partially deafferented insect interneurons. J Neurophysiol 43:367–382

    Google Scholar 

  • Nicklaus R (1965) Die Erregung einzelner Fadenhaare vonPeriplaneta americana in Abhängigkeit von der Größe und Richtung der Auslenkung. Z Vergl Physiol 50:331–362

    Google Scholar 

  • Nicon B, Poucette R, Jackson PC, Diamond J (1984) Impulse activity evoked precocious sprouting of nocioceptive nerves into denervated skin. Somatosensory Res 2:97–126

    Google Scholar 

  • Palka J, Edwards JS (1974) The cerci and abdominal giant fibers of the house cricket,Acheta domesticus. II. Regeneration and effects of chronic deprivation. Proc R Soc Lond B 185:105–121

    Google Scholar 

  • Precht W, Shimazu H, Markham CH (1966) A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J Neurophysiol 29:996–1010

    Google Scholar 

  • Shepherd D, Murphey RK (1986) Competition regulates the efficacy of an identified synapse in crickets. J Neurosci 6:3152–3160

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Vardi N (1981) Functional recovery from lesions in the escape system of the cockroach. PhD Thesis, Cornell University, Ithaca, NY

    Google Scholar 

  • Vardi N, Camhi JM (1982a) Functional recovery from lesions in the escape system of the cockroach. I. Behavioral recovery. J Comp Physiol 146:291–298

    Google Scholar 

  • Vardi N, Camhi JM (1982b) Functional recovery from lesions in the escape system of the cockroach. II. Physiological recovery of the giant interneurons. J Comp Physiol 146:299–309

    Google Scholar 

  • Volman SF (1985) Synaptic plasticity in response to partial deafferentation of giant interneurons in the American cockroach. Soc Neurosci Abstr 11:959

    Google Scholar 

  • Volman S, Camhi JM (1982) The role of activity in neuronal plasticity in the cockroach. Soc Neurosci Abstr 8:17

    Google Scholar 

  • Volman S, Camhi JM, Vardi N (1980) Role of sensory activity in behavioral recovery of the directional escape response of the cockroach. Soc Neurosci Abstr 6:679

    Google Scholar 

  • Westin J (1979) Responses to wind recorded from the cereal nerve of the cockroachPeriplaneta americana. I. Response properties of single sensory neurons. J Comp Physiol 133:97–102

    Google Scholar 

  • Westin J, Langberg JJ, Camhi JM (1977) Responses of giant interneurons of the cockroachPeriplaneta americana to wind puffs of different directions and velocities. J Comp Phyisol 121:307–324

    Google Scholar 

  • Zigmond RE, Bowers CW (1981) Influence of nerve activity on the macromolecular content of neurons and their effector organs. Annu Rev Physiol 43:673–687

    Google Scholar 

Download references

Author information

Author notes

  1. Susan F. Volman

    Present address: Division of Biology 216-76, California Institute of Technology, 91125, Pasadena, CA, USA

  2. Jeffrey M. Camhi

    Present address: Department of Zoology, Hebrew University, Jerusalem, Israel

Authors and Affiliations

  1. Section of Neurobiology and Behavior, Cornell University, 14853, Ithaca, New York, USA

    Susan F. Volman & Jeffrey M. Camhi

Authors
  1. Susan F. Volman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey M. Camhi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Volman, S.F., Camhi, J.M. The role of afferent activity in behavioral and neuronal plasticity in an insect. J. Comp. Physiol. 162, 781–791 (1988). https://doi.org/10.1007/BF00610967

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00610967

Keywords

Search

Navigation