Summary
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1.
Nine identified interneurons that originate in the 6th abdominal ganglion were studied with intracellular techniques while activating the receptors presynaptic to them with coherent water vibrations of precisely controlled amplitude and frequency. Each of the interneurons showed a characteristic response to different stimulus frequencies that was consistent from animal to animal. As a first approximation, the cells were categorized as low pass, broad band, and high pass interneurons.
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2.
Two interneurons classified as low pass interneurons (LPIs) have low thresholds to waterborne vibrations below 100 Hz, are inhibited by stimuli above 100 Hz, and respond maximally to 30 Hz stimuli.
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3.
Three interneurons classified as broad band interneurons (BBIs) respond maximally to stimuli from 30–60 Hz, but also respond well to oscillations as low as 1 Hz and as high as 80 Hz. This class is heterogeneous, spanning the range between low pass and high pass interneurons.
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4.
Two interneurons classified as high pass interneurons (HPIs) have very high thresholds to water oscillations below 6 Hz. They respond best to 60 Hz oscillations, above which their responsiveness sharply declines, although they continue to respond weakly up to 400 Hz.
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5.
Two other neurons, also classified as HPIs, responded with relatively few spikes to the stimuli we used. As a result, they do not show a clear peak responsiveness to a particular stimulus frequency.
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6.
All of the LPIs are strongly inhibited by high frequency oscillations and at least one of the phasic HPIs is inhibited at low frequencies. High frequency inhibition of LPIs can block excitatory responses to root shock, current injection and waterborne stimuli, and is due in part to postsynaptic inhibition.
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7.
Although we grouped the interneurons for analytical convenience, the frequency responses of interneurons within the groups were usually sufficiently different to allow their identification as individuals. We conclude that each interneuron's properties are precise, idiosyncratic and reproducible. These cells may be used by crayfish to analyze waterborne stimuli on the basis of frequency components.
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Abbreviations
- BBI :
-
broad band interneuron
- HRP :
-
horseradishperoxidase
- HPI :
-
high pass interneuron
- LPI :
-
low pass interneuron
References
Boyan GS (1981) Two-tone suppression of an identified auditory neurone in the brain of the cricketGryllus bimaculatus (De Geer). J Comp Physiol 114:117–125
Boyd P, Kühne R, Silver S, Lewis B (1984) Two-tone suppression and song coding by ascending neurones in the cricketGryllus campestris L. J Comp Physiol A 154:423–430
Calabrese RL (1976) Crayfish mechanoreceptive interneurons. I. The nature of ipsilateral excitatory inputs. J Comp Physiol 105:83–102
Camhi JM (1984) Neuroethology: nerve cells and the natural behavior of animals. Sinauer Associates, Sunderland Mass
Ebina Y, Wiese K (1984) A comparison of neuronal and behavioural thresholds in the displacement sensitive pathway of the crayfishProcambarus. J Exp Biol 108:45–55
Evans EF (1975) Cochlear nerve and cochlear nucleus. In: Keidel WD, Neff WD (eds) Auditory system (Handbook of sensory physiology, vol 5/2). Springer, Berlin Heidelberg New York, pp 1–108
Hergenröder R, Barth FG (1983) The release of attack and escape behavior by vibratory stimuli in a wandering spider (Cupiennius salei Keys). J Comp Physiol 152:347–358
Hutchings M, Lewis B (1984) The role of two-tone suppression in song coding by ventral cord neurones in the cricketTeleogryllus océanicus (Le Guillou). J Comp Physiol 154:103–112
Kämper G (1984) Abdominal ascending interneurons in crickets: responses to sound at 30-Hz calling-song frequency. J Comp Physiol A 155:507–520
Kanou M, Shimozawa T (1984) A threshold analysis of cricket cereal interneurons by an alternating air-current stimulus. J Comp Physiol A 154:357–365
Kennedy D (1971) Crayfish interneurons. Physiologist 14:5–30
Lang HH (1980) Surface wave discrimination between prey and nonprey by the backswimmerNotonecta glauca L. (Hemiptera, Heteroptera). Behav Ecol Sociobiol 6:233–246
Larimer JL, Jellies J (1983) The organization of flexion-evoking interneurons in the abdominal nerve cord of the crayfish,Procambarus clarkii. J Exp Biol 226:341–351
Levine RB, Murphey RK (1980) Pre- and postsynaptic inhibition of identified giant interneurons in the cricket (Acheta domesticus). J Comp Physiol 135:269–282
Miall RC, Larimer JL (1982) Interneurons involved in abdominal posture in crayfish: structure, function and command fiber responses. J Comp Physiol 148:159–173
Moiseff A, Hoy RR (1983) Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible link to phonotactic behavior. J Comp Physiol 152:155–167
Murphey RK, Palka J, Hustert R (1977) The cercus-to-giant interneuron system of crickets. II. Response characteristics of two giant interneurons. J Comp Physiol 119:285–300
Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: the role of behavioral context. Science 226:992–994
Plummer MR (1984) Frequency coding of waterborne vibrations by the crayfish. PhD Dissertation. Stanford University
Plummer MR, Camhi JM (1981) Discrimination of sensory signals from noise in the escape system of the cockroach: the role of wind acceleration. J Comp Physiol 142:347–357
Plummer MR, Tautz J, Wine JJ (1982) Response properties and output effects of identified mechanosensory interneurons in the crayfish,Procambarus clarkii. Neurosci Abstr 8:688
Reichert H, Plummer MR, Hagiwara G, Roth RL, Wine JJ (1982) Local interneurons in the terminal abdominal ganglion of the crayfish. J Comp Physiol 149:145–162
Ritzmann RE, Tobias ML, Fourtner CR (1980) Flight activity initiated via giant interneurons of the cockroach: evidence for bifunctional trigger neurons. Science 210:443–445
Shimozawa T, Kanou M (1984) Varieties of filiform hairs: range fractionation by sensory afferents and cereal interneurons of a cricket. J Comp Physiol A 155:485–493
Sigvardt KA, Hagiwara G, Wine JJ (1982) Mechanosensory integration of the crayfish abdominal nervous system: structural and physiological differences between interneurons with single and multiple spike initiating sites. J Comp Physiol 148:143–157
Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759
Tautz J (1979) Reception of particle oscillation in a mediuman unorthodox sensory capacity. Naturwissenschaften 66:452–461
Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to airborne vibration. Behav Ecol Sociobiol 4:101–110
van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–432
Wiersma CAG, Hughes GM (1961) On the functional anatomy of neuronal units in the abdominal cord of the crayfish,Procambarus clarkii (Girard). J Comp Neurol 116:209–228
Wiese K, Calabrese RL, Kennedy D (1976) Integration of directional mechanosensory input by crayfish interneurons. J Neurophysiol 39:834–843
Wine JJ, Krasne FB (1982) The cellular organization of crayfish escape behavior. In: Bliss DE (ed) The biology of Crustacea, vol 4. Academic Press, New York, pp 241–292
Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricketGryllus campestris L. J Comp Physiol 146:161–173
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Plummer, M.R., Tautz, J. & Wine, J.J. Frequency coding of waterborne vibrations by abdominal mechanosensory interneurons in the crayfish,Procambarus clarkii . J. Comp. Physiol. 158, 751–764 (1986). https://doi.org/10.1007/BF01324819
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DOI: https://doi.org/10.1007/BF01324819