Skip to main content
SpringerLink
Log in

Morphological correlates of pyramidal cell adaptation rate in the electrosensory lateral line lobe of weakly electric fish

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

Summary

  1. 1.

    Extracellular HRP injections into the nucleus praeeminentialis dorsalis (NPd) ofApteronotus leptorhynchus retrogradely labeled a population of elec trosensory lateral line lobe (ELL) efferent cells, deep basilar pyramidal cells, that differ morphologically from the previously described basilar and nonbasilar pyramidal cells. These neurons are found deep in the ELL cellular layers; they have small cell bodies and very short sparsely branching apical dendritic trees. The previously described basilar and nonbasilar pyramidal cells are larger, have extensive apical dendrites and are found more superficially.

  2. 2.

    Axon terminals of the deep basilar pyramidal cells were recorded from in the NPd and labeled with lucifer yellow. These NPd afferents have high, regular spontaneous firing rates, and respond tonically to changes in electric organ discharge amplitude.

  3. 3.

    Deep basilar pyramidal cell bodies were recorded from and labeled in the ELL, and these showed the same physiological responses as did the NPd afferent fibers.

  4. 4.

    In addition, basilar pyramidal cells were found which had spontaneous activity patterns and adaptation characteristics intermediate to those typical of the superficial basilar pyramidal cells and the deep basilar pyramidal cells. The size of the pyramidal cells' apical dendritic trees and the placement of their somata within the dorsoventral extent of the ELL cellular layers are highly correlated with the neurons' physiological properties.

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.

Similar content being viewed by others

Abbreviations

BP :

basilar pyramidal cell

DBP :

deep basilar pyramidal cell

EGp :

eminentia granularis posterior

ELL :

electrosensory lateral line lobe

EOD :

electric organ discharge

GABA :

gamma amino butyric acid

HRP :

horseradish peroxidase

NBP :

non basilar pyramidal cell

NMDA :

N-methyl-D-aspartate

NPd :

nucleus praeeminentialis dorsalis

PSTH :

post stimulus time histogram

TSF :

tractus strati fibrosi

References

  • Bastian J (1981a) Electrolocation I: An analysis of the effects of moving objects and other electrical stimuli on the electroreceptor activity ofApteronotus albifrons. J Comp Physiol 144:465–479

    Google Scholar 

  • Bastian J (1981b) Electrolocation II: The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells inApteronotus albifrons. J Comp Physiol 144:481–494

    Google Scholar 

  • Bastian J (1986a) Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6:553–562

    CAS  PubMed  Google Scholar 

  • Bastian J (1986b) Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe. J Comp Physiol A 158:505–515

    Article  CAS  PubMed  Google Scholar 

  • Bastian J (1986c) Electrolocation: Behavior, anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 577–612

    Google Scholar 

  • Bastian J (1990) Electroreception. In: Stebbins WC, Berkley MA (eds) Comparative perception, complex signals, vol II. Wiley, New York, pp 35–89

    Google Scholar 

  • Bastian J, Bratton B (1990) Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe, J Neurosci 10:1226–1240

    CAS  PubMed  Google Scholar 

  • Bratton B, Bastian J (1990) Descending control of electroreception II: Properties of nucleus praeeminentialis neurons projecting directly to the electrosensory lateral line lobe. J Neurosci 10:1241–1253

    CAS  PubMed  Google Scholar 

  • Carr CE, Maler L (1986) Electroreception in gymnotiform fish: Central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–373

    Google Scholar 

  • Carr CE, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of gymnotiform fish: Morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203:649–670

    Article  CAS  PubMed  Google Scholar 

  • Carr CE, Maler L, Sas E (1982) Peripheral and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211:139–153

    Article  CAS  PubMed  Google Scholar 

  • Enger PS, Szabo T (1965) Activity of central neurons involved in electroreception in some weakly electric fish (Gymnotidae). J Neurophysiol 28:800–818

    CAS  PubMed  Google Scholar 

  • Hablitz JJ, Mistry DK (1990) NMDA-evoked outward currents in cultured neocortical neurons using nystatin-perforated patch recordings. Soc Neurosci Abstr 16:1184

    Google Scholar 

  • Heiligenberg W (1977) Principles of electrolocation and jamming avoidance. In: Braitenberg V (ed) Studies of Brain Function, vol 1. Springer, Berlin Heidelberg New York, pp 1–85

    Google Scholar 

  • Heiligenberg W (1986) Jamming avoidance systems: Model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–649

    Google Scholar 

  • Heiligenberg WH, Dye J (1982) Labelling of electroreceptor afferents in a gymnotoid fish by intracellular injection of HRP: The mystery of multiple maps. J Comp Physiol 148:287–296

    Article  Google Scholar 

  • Hill RH, Brodin L, Grillner S (1989) Activation of N-methyl-D-aspartate (NMDA) receptors augments repolarizing responses in lamprey spinal neurons. Brain Res 499:388–392

    Article  CAS  PubMed  Google Scholar 

  • Larkman A, Mason A (1990) Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes. J Neurosci 10:1407–1414

    CAS  PubMed  Google Scholar 

  • Maler L (1979) The posterior lateral line lobe of certain gymnotoid fish: Quantitative light microscopy. J Comp Neurol 183:323–364

    Article  CAS  PubMed  Google Scholar 

  • Maler L, Monoghan D (1989) Distribution of glutamate receptors in the electrosensory system of gymnotiform fish. Soc Neurosci Abstr 15:1135

    Google Scholar 

  • Maler L, Mugnaini E (1986) Immunohistochemical identification of GABAergic synapses in the electrosensory lateral line lobe of a weakly electric fish (Apteronotus leptorhynchus). Soc Neurosci Abstr 12:312

    Google Scholar 

  • Maler L, Sas EKB, Rogers J (1981) The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (Gymnotidae): Dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neurol 195:87–139

    Article  CAS  PubMed  Google Scholar 

  • Maler L, Sas E, Carr C, Matsubara J (1982) Efferent projections of the posterior lateral line lobe in gymnotiform fish. J Comp Neurol 211:154–164

    Article  CAS  PubMed  Google Scholar 

  • Mason A, Larkman A (1990) Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J Neurosci 10:1415–1428

    CAS  PubMed  Google Scholar 

  • Mathieson WB, Maler L (1988) Morphological and electrophysiological properties of a novel in vitro preparation: The electrosensory lateral line lobe brain slice. J Comp Physiol A 163:489–506

    Article  CAS  PubMed  Google Scholar 

  • Metcalf WK (1985) Wsensory neuron growth cones comigrate with posterior lateral line lobe primordial cells in zebrafish. J Comp Neurol 238:218–224

    Google Scholar 

  • Nadi S, Maler L (1987) The laminar distribution of amino acids in the caudal cerebellum and electrosensory lateral line lobe of weakly electric fish (Gymnotidae). Brain Res 425:218–224

    Article  CAS  PubMed  Google Scholar 

  • Réthelyi M, Szabo T (1973) Neurohistological analysis of the lateral line lobe in a weakly electric fish,Gymnotus carapo (Gymnotidae, Pisces). Exp Brain Res 18:323–339

    Article  PubMed  Google Scholar 

  • Sas E, Maler L (1983) The nucleus praeeminentialis: A Golgi study of a feedback center in the electrosensory system of gymnotid fish. J Comp Neurol 221:127–144

    Article  CAS  PubMed  Google Scholar 

  • Sas E, Maler L (1987) The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fishApteronotus leptorhynchus. Anat Embryol 177:55–79

    Article  CAS  PubMed  Google Scholar 

  • Saunders J, Bastian J (1984) The physiology and morphology of two types of electrosensory neurons in the weakly electric fishApteronotus leptorhynchus. J Comp Physiol A 154:199–209

    Google Scholar 

  • Schwindt PC, Spain WJ, Foehring RC, Stafstrom CE, Chubb MC, Crill WE (1988a) Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 59:424–449

    CAS  PubMed  Google Scholar 

  • Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988b) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol 59:450–467

    CAS  PubMed  Google Scholar 

  • Shumway CA (1990a) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I: Physiological differences. J Neurosci 9:4388–4399

    Google Scholar 

  • Shumway CA (1990b) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II: Anatomical differences. J Neurosci 9:4400–4415

    Google Scholar 

  • Shumway CA, Maler L (1989) GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish. J Comp Physiol A 164:391–407

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. W. H. Freeman and Company, San Francisco, pp 114–117

    Google Scholar 

  • Turner RW, Maler L (1989) Synaptic plasticity in the cerebellar parallel fiber projection to the electrosensory lateral line lobe of gymnotiform fish. Soc Neurosci Abstr 15:1135

    Google Scholar 

  • Zakon HH (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 103–156

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Oklahoma, Norman, 73019, OK, USA

    Joseph Bastian & Jay Courtright

Authors
  1. Joseph Bastian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jay Courtright
    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

Bastian, J., Courtright, J. Morphological correlates of pyramidal cell adaptation rate in the electrosensory lateral line lobe of weakly electric fish. J Comp Physiol A 168, 393–407 (1991). https://doi.org/10.1007/BF00199600

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00199600

Key words

Search

Navigation