Frequency coding of waterborne vibrations by abdominal mechanosensory interneurons in the crayfish, Procambarus clarkii

Mark Plummer, Jürgen Tautz, Jeffrey J. Wine

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Abstract

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. 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. 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. 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. 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. 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. 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.

Original languageEnglish (US)
Pages (from-to)751-764
Number of pages14
JournalJournal of Comparative Physiology A Sensory, Neural, and Behavioral Physiology
Volume158
Issue number6
DOIs
StatePublished - Nov 1 1986

Fingerprint

Astacoidea
Procambarus clarkii
interneurons
Interneurons
crayfish
Vibration
vibration
oscillation
animal
water
Presynaptic Receptors
abdominal ganglia
Water

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Animal Science and Zoology
  • Physiology
  • Behavioral Neuroscience

Cite this

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title = "Frequency coding of waterborne vibrations by abdominal mechanosensory interneurons in the crayfish, Procambarus clarkii",
abstract = "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. 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. 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. 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. 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. 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. 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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N2 - 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. 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. 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. 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. 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. 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. 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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