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Journal of Comparative Physiology A

, Volume 164, Issue 3, pp 391–407 | Cite as

GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish

  • Caroly A. Shumway
  • Leonard Maler
Article

Summary

  1. 1.

    The amplitude-coding pyramidal neurons of the first-order nucleus in weakly electric gymnotiform fish (Eigenmannia), the electrosensory lateral line lobe (ELL), exhibit 2 major physiological transformations of primary afferent input. Pyramidal cells rapidly adapt to a step change in amplitude, and they have a center/surround receptive-field organization. This study examined the physiological role of GABAergic inhibition on pyramidal cells. GABAergic synapses onto the somata of pyramidal cells primarily originate from granule-cell interneurons along with descending input.

     
  2. 2.

    Pyramidal cells fall into two physiologically distinct categories: E units, which are excited by a rise in stimulus amplitude, and I units, which are inhibited by a rise in stimulus amplitude. Microiontophoretic application of bicuculline methiodide onto both types of pyramidal cells increased the time constant of adaptation, defined as the time required for the neuron's response to decay to 37% of its maximum value, by 70–90%. The peak firing rate of E units to a step increase in stimulus amplitude increased by 49%, while the firing rate of I units did not change significantly.

     
  3. 3.

    Bicuculline application demonstrated that GABAergic inhibition may contribute to the strict segregation of E and I response properties. In the presence of bicuculline, many E units (normally excited only by stimulus amplitude increases) became excited by both increases and decreases; many I units (normally excited only by amplitude decreases) also became excited to increases.

     
  4. 4.

    The size of the excitatory receptive-field of E units was not affected by bicuculline, although response magnitude increased. The inhibitory surround increased in spatial extent by 175% with bicuculline administration. Neither the size of the I unit receptive-field center nor the response magnitude changed in the presence of bicuculline. The antagonistic surround of I units, however, increased by 49%.

     
  5. 5.

    The anatomy of the ELL is well understood (see Carr and Maler 1986). The physiological results obtained in this study, along with the results of Bastian (1986a, b), further our understanding of the functional role of the ELL circuitry. Our results suggest that spatial and temporal response properties of pyramidal cells are regulated by different but interacting inhibitory interneurons, some of which use GABA as a neurotransmitter (see Figs. 11 and 12). The activity of these interneurons is in turn controlled by descending feedback systems.

     

Keywords

Pyramidal Cell Bicuculline Stimulus Amplitude GABAergic Inhibition Methiodide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ELL

electrosensory lateral line lobe

EOD

electric organ discharge

NPd

dorsal nucleus praeeminentialis

EGP

eminentia granularis posterior

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Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Caroly A. Shumway
    • 1
  • Leonard Maler
    • 2
  1. 1.Neurobiology Unit A-002, Scripps Institution of OceanographyUniversity of CaliforniaSan Diego, La JollaUSA
  2. 2.Department of Anatomy, Faculty of Health SciencesUniversity of OttawaOttawaCanada

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