Journal of Comparative Physiology A

, Volume 174, Issue 4, pp 399–410 | Cite as

Processing of mechanosensory information from gustatory receptors on a hind leg of the locust

  • P. L. Newland
  • M. Burrows
Article

Abstract

Gustatory receptors (basiconic sensilla) on the legs of the desert locust, Schistocerca gregaria, are innervated by chemosensory afferents and by a mechanosensory afferent. We show, for the first time, that these mechanosensory afferents form an elaborate detector system with the following properties: 1) they have low threshold displacement angles that decrease with increasing stimulus frequency in the range 0.05–1 Hz, 2) they respond phasically to deflections of the receptor shaft and adapt rapidly to repetitive stimulation, 3) they encode the velocity of the stimulus in their spike frequency and have velocity thresholds lower than 1°/s, and 4) they are directionally sensitive, so that stimuli moving proximally towards the coxa elicit the greatest response.

The mechanosensory afferents, but not the chemosensory afferents, make apparently monosynaptic connections with spiking local interneurones in a population with somata at the ventral midline of the metathoracic ganglion. They evoke excitatory synaptic potentials that can sum to produce spikes in the spiking local interneurones. Stimulation of the single mechanosensory afferent of a gustatory receptor can also give rise to long lasting depolarizations, or to bursts of excitatory postsynaptic potentials in the interneurones that can persist for several seconds after the afferent spikes. These interneurones are part of the local circuitry involved in the production of local movements of a leg. The mechanosensory afferents from gustatory receptors must, therefore, be considered as part of the complex array of exteroceptors that provide mechanosensory information to these local circuits for use in adjusting, or controlling locomotion.

Key words

Locust Basiconic sensilla Mechanoreception Chemoreception Spiking local interneurones 

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References

  1. Bacon JP, Murphey RK (1984) Receptive fields of cricket giant interneurones are related to their dendritic structure. J Physiol (Lond) 352:601–623Google Scholar
  2. Blaney WM (1974) Electrophysiological responses of the terminal sensilla on the maxillary palps of Locusta migratoria (L.) to some electrolytes and non-electrolytes. J Exp Biol 60:275–293Google Scholar
  3. Blaney WM (1975) Behavioural and electrophysiological studies of taste discrimination by the maxillary palps of the larvae of Locusta migratoria (L.). J Exp Biol 62:555–569Google Scholar
  4. Blaney WM, Chapman RF (1969) The fine structure of the terminal sensilla on the maxillary palps of Schistocerca gregaria (Forskål) (Orthoptera, Acrididae). Z Zellforsch 99:74–97Google Scholar
  5. Buño W, Monti-Bloch L, Crispino L (1981) Dynamic properties of cockroach cereal “bristlelike” hair sensilla. J Neurobiol 12:101–121Google Scholar
  6. Burrows M (1985) The processing of mechanosensory information by spiking local interneurons in the locust. J Neurophysiol 54:463–478Google Scholar
  7. Burrows M (1987) Parallel processing of proprioceptive signals by spiking local interneurons and motor neurons in the locust. J Neurosci 7:1064–1080Google Scholar
  8. Burrows M (1992a) Reliability and effectiveness of transmission from exteroceptive sensory neurones to spiking local interneurones in the locust. J Neurosci 12:1477–1489Google Scholar
  9. Burrows M (1992b) Local circuits for the control of leg movements in an insect. Trends Neurosci 15:226–232Google Scholar
  10. Burrows M, Newland PL (1993) Correlation between the receptive fields of locust interneurons, their dendritic morphology, and the central projections of mechanosensory neurons. J Comp Neurol 329:412–426Google Scholar
  11. Burrows M, Siegler MVS (1984) The morphological diversity and receptive fields of spiking local interneurones in the locust metathoracic ganglion. J Comp Neurol 224:483–508Google Scholar
  12. Burrows M, Laurent GJ, Field LH (1988) Proprioceptive inputs to nonspiking local interneurons contribute to local reflexes of a locust hindleg. J Neurosci 8:3085–3093Google Scholar
  13. Burrows M, Watson AHD, Brunn DE (1989) Physiological and ultrastructural characterization of a central synaptic connection between identified motor neurons in the locust. Europ J Neurosci 1:111–126Google Scholar
  14. Chapman RF (1982) Chemoreception: the significance of receptor numbers. Adv Insect Physiol 16:247–356Google Scholar
  15. Dethier VG (1972) Sensitivity of the contact chemoreceptors of the blowfly to vapors. Proc Natl Acad Sci USA 69:2189–2192Google Scholar
  16. Dethier VG (1976) The hungry fly. A physiological study of the behavior associated with feeding. Harvard University Press, CambridgeGoogle Scholar
  17. Drewes CD, Bernard RA (1976) Electrophysiological responses of chemosensitive sensilla in the wolf spider. J Exp Zool 198:423–435Google Scholar
  18. Hodgson ES, Lettvin JY, Roeder KD (1955) Physiology of a primary chemoreceptor unit. Science 122:417–418Google Scholar
  19. Kendall MD (1970) The anatomy of the tarsi of Schistocerca gregaria Forskål. Z Zellforsch 109:112–137Google Scholar
  20. Klein U (1981) Sensilla of the cricket palp. Fine structure and spatial organization. Cell Tissue Res 219:229–252Google Scholar
  21. Kondoh Y, Arima T, Okuma J, Hasegawa Y (1991) Filter characteristics of cereal afferents in the cockroach. J Comp Physiol A 169:653–662Google Scholar
  22. Laurent GJ, Burrows M (1988a) Direct excitation of nonspiking local interneurones by exteroceptors underlies tactile reflexes in the locust. J Comp Physiol A 162:563–572Google Scholar
  23. Laurent G, Burrows M (1988b) A population of ascending intersegmental interneurones in the locust with mechanosensory inputs from a hind leg. J Comp Neurol 275:1–12Google Scholar
  24. Laurent GJ, Hustert R (1988) Motor neuronal receptive fields delimit patterns of activity during locomotion of the locust. J Neurosci 8:4349–4366Google Scholar
  25. Matheson T (1992) Morphology of the central projections of physiologically characterised neurones from the locust metathoracic femoral chordotonal organ. J Comp Physiol A 170:101–120Google Scholar
  26. Mitchell BK, Itagaki H (1992) Interneurons of the subesophageal ganglion of Sarcophaga bullata responding to gustatory and mechanosensory stimuli. J Comp Physiol A 171:213–230Google Scholar
  27. Murphey, RK, Bacon JP, Johnson SE (1985) Ectopic neurons and the organization of insect sensory systems. J Comp Physiol A 156:381–389Google Scholar
  28. Murphey RK, Possidente D, Pollack G, Merritt D (1989) Modality-specific axonal organization of insect sensory systems. J Comp Neurol 290:185–200Google Scholar
  29. Nagayama T (1989) Morphology of a new population of spiking local interneurones in the locust metathoracic ganglion. J Comp Neurol 283:189–211Google Scholar
  30. Nagayama T, Burrows M (1990) Input and output connections of an anteromedial group of spiking local interneurones in the metathoracic ganglion of the locust. J Neurosci 10:785–794Google Scholar
  31. Newland PL (1990) The morphology of a population of mechanosensory ascending interneurones in the metathoracic ganglion of the locust. J Comp Neurol 299:242–260Google Scholar
  32. Newland PL (1991a) Physiological properties of tactile hair afferents on the hind leg of the locust. J Exp Biol 155:487–503Google Scholar
  33. Newland PL (1991b) Morphology and somatotopic organisation of the central projections of afferents from tactile hairs on the hind leg of the locust. J Comp Neurol 311:1–16Google Scholar
  34. Palka J, Levine R, Schubiger M (1977) The cercus-to-giant interneuron system of crickets. I. Some attributes of the sensory cells. J Comp Physiol 119:267–283Google Scholar
  35. Pflüger HJ (1980) The function of hair sensilla on the locust's leg: the role of tibial hairs. J Exp Biol 87:163–175Google Scholar
  36. Pflüger HJ, Bräunig P, Hustert R (1988) The organisation of mechanosensory neuropiles in locust thoracic ganglia. Phil Trans R Soc Lond 321:1–26Google Scholar
  37. Siegler MVS, Burrows M (1983) Spiking local interneurons as primary integrators of mechanosensory information in the locust. J Neurophysiol 50:1281–1295Google Scholar
  38. Siegler MVS, Burrows M (1984) The morphology of two groups of spiking local interneurons in the metathoracic ganglion of the locust. J Comp Neurol 224:463–4482Google Scholar
  39. Siegler MVS, Burrows M (1986) Receptive fields of motor neurons underlying local tactile reflexes in the locust. J Neurosci 6:507–513Google Scholar
  40. Simpson SJ (1992) Mechanoresponsive neurones in the sub-oesophageal ganglion of the locust. Physiol Entomol 17:351–369Google Scholar
  41. Shimozawa T, Kanou M (1984) Varieties of filiform hairs: range fractionation by sensory afferents and cereal interneurons of a cricket. J Comp Physiol A 155:485–493Google Scholar
  42. Städler E, Hanson FE (1975) Olfactory capabilities of the “gustatory” chemoreceptors of the tobacco hornworm larvae. J Comp Physiol 104:97–102Google Scholar
  43. Tautz J (1978) Reception of medium vibration by thoracal hairs of caterpillars of Barathra brassicae L. (Lepidoptera, Noctuidae). II. Response characteristics of the sensory cell. J Comp Physiol 125:67–77Google Scholar
  44. Trimmer BA, Weeks JC (1991) Activity-dependent induction of facilitation, depression, and post-tetanic potentiation at an insect central synapse. J Comp Physiol A 168:27–43Google Scholar
  45. Westin J (1979) Responses to wind recorded from the cereal nerve of the cockroach Periplaneta americana. I. Response properties of single sensory neurons. J Comp Physiol 133:97–102Google Scholar
  46. White PR, Chapman RF (1990) Tarsal chemoreception in the polyphagous grasshopper Schistocerca americana: behavioural assays, sensilla distributions and electrophysiology. Physiol Entomol 15:105–121Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • P. L. Newland
    • 1
  • M. Burrows
    • 1
  1. 1.Department of ZoologyUniversity of CambridgeCambridgeUK

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