Skip to main content
SpringerLink
Log in

Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice

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

Summary

An in vitro brain slice preparation of the electrosensory lateral line lobe (ELL) of weakly electric fish was developed. The morphology of this slice was studied and revealed that most ELL neurons and synapses retained their normal appearance for at least 10 h in vitro. The electrophysiological characteristics of the main ELL output neurons, the pyramidal cells, were measured. Extracellular electrode recordings demonstrated that pyramidal cells are capable of spontaneous, rhythmic spike activity. Intracellular recordings showed that intrinsic oscillations in membrane potential underlie the bursting behavior. The majority of pyramidal cells respond to depolarizing current pulses with an initial lag in spike firing followed by a non-accommodating, higher frequency spike train.

Time and voltage-dependent properties of pyramidal cell responsiveness, as well as the effects of pharmacological blocking agents indicated that rhythmic activity and repetitive firing are dominated by a persistent, subthreshold sodium conductance (gNa) which activates at depolarized levels and is the driving force behind the membrane potential oscillations and the sustained (non-accommodating) spike firing. In addition, a transient, outward potassium conductance (gA) is responsible for the lag in spike firing by acting as a ‘brake’ during the initial 50–200 ms of a depolarizing stimulus.

Calcium currents and calcium-dependent potassium conductance add to the interval between spontaneous bursts but appear insufficient for spike frequency accommodation.

The in vitro behaviour of pyramidal cells differs substantially from the behaviour of the same cell type in vivo. These observations raise possibilities that intrinsic membrane properties together with local synaptic interactions may regulate pyramidal cell responsiveness.

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.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ACSF :

artificial cerebrospinal fluid

4-AP :

4-amino-pyridine

BP :

basilar pyramidal cell

DML :

dorsal molecular layer

EGTA :

ethyleneglycol-bis(B-aminoethylether)-N,N′tetraacetic acid

ELL :

electrosensory lateral line lobe

EOD :

electric organ discharge

EPSP :

excitatory postsynaptic potential

FPP :

fast prepotential

IPSP :

inhibitory postsynaptic potential

LF :

Lucifer Yellow

NBP :

non-basilar pyramidal cell

Rin :

input resistance

SP :

slow potential

TEA :

tetraethyl ammonium

tsf :

tractus stratum fibrosum

TTX :

tetrodotoxin

Vm :

membrane potential

VML :

ventral molecular layer

References

  • Bagust J, Kerkut GA (1980) The use of the transition elements manganese, cobalt, and nickel as synaptic blocking agents on isolated, hemisected, mouse spinal cord. Brain Res 182:474–477

    Google Scholar 

  • Bastian J (1981a) Electrolocation. I. How the electroreceptors ofApteronotus albifrons code for moving objects and other electrical stimuli. J Comp Physiol 144:456–479

    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 6:533–562

    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 158:505–516

    Google Scholar 

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

    Google Scholar 

  • Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299–1301

    Google Scholar 

  • Connor JA, Stevens CF (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural soma. J Physiol 213:21–30

    Google Scholar 

  • Connors BW, Kriegstein AR (1986) Cellular physiology of the turtle visual cortex: Distinctive properties of pyramidal and stellate neurons. J Neurosci 6:164–177

    Google Scholar 

  • Eccles JC (1964) The physiology of synapses. Springer, Berlin Heidelberg New York, pp 173–188

    Google Scholar 

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

    Google Scholar 

  • Gerhardt SC, Bernard P, Pastor G, Boast CA (1986) Effects of systemic administration of the NMDA antagonist, CPP, on ischemic brain damage in gerbils. Neurosci Abstr 12:59

    Google Scholar 

  • Grace AA, Llinás R (1985) Morphological artifacts induced in intracellularly stained neurons by dehydration: circumvention using rapid dimethyl sulfoxide clearing. Neurosci 16:461–476

    Google Scholar 

  • Heiligenberg W, Dye J (1982) Labelling of electroreceptive afferents in a gymnotid fish by intracellular injection of HRP: the mystery of multiple maps. J Comp Physiol 148:287–296

    Google Scholar 

  • Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol 111: 171–207

    Google Scholar 

  • Hugues M, Romey G, Duval D, Vincent JP, Lazsunski M (1982) Apamin as a selective blocker of the calcium-dependent potassium channel in neuroblastoma cells: voltageclamp and biochemical characterization of the toxin receptor. Proc Natl Acad Sci USA 79:1308–1312

    Google Scholar 

  • Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells. Clarendon Press, Oxford

    Google Scholar 

  • Knudsen E (1974) Spatial aspects of the electric fields generated by weakly electric fish. J Comp Physiol 99:103–118

    Google Scholar 

  • MacVicar BA, Dudek FE (1980) Dye-coupling between CA3 pyramidal cells in slices of rat hippocampus. Brain Res 196:494–497

    Google Scholar 

  • MacVicar BA, Dudek FE (1981) Electronic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213:782–784

    Google Scholar 

  • Madison DV, Nicoll RA (1982) Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299:636–638

    Google Scholar 

  • Maler L (1979) The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J Comp Neurol 183:323–363

    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 84:312

    Google Scholar 

  • Maler L, Collins M, Mathieson WB (1981a) The distribution of acetylcholinesterase and choline acetyl transferase in the cerebellum and posterior lateral line lobe of weakly electric fish (Gymnotidae). Brain Res 226:320–325

    Google Scholar 

  • Maler L, Sas E, Rogers J (1981b) 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

    Google Scholar 

  • Mathieson WB, Heiligenberg W, Maler L (1986) Ultrastructural studies of synaptic targets of physiologically identified electrosensory afferent synapses in the gymnotiform fish,Eigenmannia. J Comp Neurol 255:526–537

    Google Scholar 

  • McLennan H (1983) Receptors for the excitatory amino acids in the central nervous system. Prog Neurobiol 20:251–271

    Google Scholar 

  • Matsubara J (1981) Neural correlates of a nonjammable electrolocation system. Science 211:722–1725

    Google Scholar 

  • Meldrum MJ, Chroucher G, Badman G, Coffins JF (1983) Antiepileptic action of excitatory amino acid antagonists in the photosensitive baboon,Papio papio. Neurosci Lett 39:101–104

    Google Scholar 

  • Milan F, Janigro D, DiGregorio D, Gorio A (1985) GM1 treatment in vivo protects membrane ATPase activities and prevents mitochondrial damage in hippocampal slices. Neurosci Abstr 11:376

    Google Scholar 

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

    Google Scholar 

  • Neher E (1971) Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol 58:36–53

    Google Scholar 

  • Nakajima Y, Nakajima S, Leonard RS, Yamaguchi K (1986) Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc Natl Acad Sci USA 83:3022–3026

    Google Scholar 

  • Partridge BL, Heiligenberg W, Matsubara J (1981) The neural basis of a sensory filter in the jamming avoidance response: no grandmother cells in sight. J Comp Physiol 145:153–163

    Google Scholar 

  • Phan M, Maler L (1983) Distribution of muscarinic receptors in the caudal cerebellum and electrosensory lateral line lobe of gymnotiform fish. Neurosci Lett 42:137–143

    Google Scholar 

  • Rogawski MA (1985) The A current: how ubiquitous a feature of excitable cells is it? Trends Neurosci 8:214–219

    Google Scholar 

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

    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 

  • Scheich H (1977) Neural basis of communication in the high frequency electric fish,Eigenmannia virescens (jamming avoidance response). J Comp Physiol 113:181–255

    Google Scholar 

  • Scheich H, Bullock TH, Hamstra RH (1973) Coding properties of two classes of afferent nerve fibers: high frequency electroreceptors in the electric fish,Eigenmannia. J Neurophysiol 36:39–60

    Google Scholar 

  • Schubert P, Mitzdorf U (1979) Analysis and quantitative evaluation of the depressive effect of adenosine on evoked potentials in hippocampal slices. Brain Res 172:186–190

    Google Scholar 

  • Schwartzkroin PA (1977) Further characteristics of hippocampal CA1 cells in vitro. Brain Res 128:53–68

    Google Scholar 

  • Shumway CA, Maler L (in press) Bicucculine affects both temporal and receptive field properties of pyramidal cells in the electrosensory lateral line lobe. Soc Neurosci Abstr

  • Spencer WA, Kandel ER (1961) Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J Neurophysiol 24:272–285

    Google Scholar 

  • Stafstrom CE, Schwindt PC, Flatman JA, Crill WE (1984) Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol 52:224–263

    Google Scholar 

  • Thompson SH (1977) Three pharmacologically distinct potassium channels in molluscan neurons. J Physiol 265:465–488

    Google Scholar 

  • van Herreveld A, Stamm JS (1953) Effect of pentobarbitol and ether on the spreading cortical depression. Am J Physiol 173:164–170

    Google Scholar 

  • Zbicz KL, Weight FF (1985) Transient voltage and calcium-dependent outward currents in hippocampal CA3 pyramidal neurons. J Neurophysiol 53:1038–1057

    Google Scholar 

Download references

Author information

Author notes

  1. William B. Mathieson

    Present address: Department of Medical Physiology, Faculty of Medicine, University of Calgary, 3330 Hospital Dr., N.W., T2N 4N1, Calgary, Alberta, Canada

Authors and Affiliations

  1. Department of Anatomy, Faculty of Health Sciences, University of Ottawa, K1H 8M5, Ottawa, Canada

    William B. Mathieson & Leonard Maler

Authors
  1. William B. Mathieson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonard Maler
    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

Mathieson, W.B., Maler, L. Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J. Comp. Physiol. 163, 489–506 (1988). https://doi.org/10.1007/BF00604903

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00604903

Keywords

Search

Navigation