The Mormyrid Electrosensory Lobe In Vitro: Physiology and Pharmacology of Cells and Circuits

This paper is concerned with the electrosensory lobe (ELL) of mormyrid electric fish as examined in in vitro slices. Intracellular recordings from morphologically identified cells and field potential recordings were used to characterize the physiology and pharmacology of ELL cells. Most intracellular recordings were from the Purkinje-like interneurons that are known as medium ganglion cells and from the two types of efferent neurons, large ganglion and large fusiform cells. Stimulation of primary afferent fibers elicits both excitatory and inhibitory effects in these cells, with the excitatory effects being mediated by both the AMPA and NMDA types of glutamate receptors and the inhibitory effects being mediated by both GABAA and glycine receptors. Parallel-fiber stimulation evokes an EPSP–IPSP sequence, with the EPSPs being mediated by both AMPA and NMDA receptors and the IPSPs being mediated by GABAA receptors only. The parallel fiber-evoked EPSPs and IPSPs show marked paired-pulse facilitation. A large and unusually broad spike is recorded inside medium ganglion cells, and field potential responses suggest that this spike is propagated into the apical dendrites. The results provide essential information for understanding how peripheral and central inputs are integrated in ELL.

[1]  K. Grant,et al.  Physiology and Plasticity of Morphologically Identified Cells in the Mormyrid Electrosensory Lobe , 1997, The Journal of Neuroscience.

[2]  K. Grant,et al.  Projection neurons of the mormyrid electrosensory lateral line lobe: Morphology, immunohistochemistry, and synaptology , 1996, The Journal of comparative neurology.

[3]  R. Petralia,et al.  Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus , 1996, The Journal of comparative neurology.

[4]  D. Bodznick,et al.  The Specificity of an Adaptive Filter That Suppresses Unwanted Reafference in Electrosensory Neurons of the Skate Medulla. , 1993, The Biological bulletin.

[5]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[6]  C. Bell,et al.  The generation and subtraction of sensory expectations within cerebellum-like structures. , 1997, Brain, behavior and evolution.

[7]  R. Llinás,et al.  Electrophysiological analysis of synaptic transmission , 1969 .

[8]  L. Maler,et al.  Excitatory amino acid receptors at a feedback pathway in the electrosensory system: implications for the searchlight hypothesis. , 1997, Journal of neurophysiology.

[9]  Clay Armstrong,et al.  Synaptically triggered action potentials in dendrites , 1993, Neuron.

[10]  P. Somogyi,et al.  Colocalization of glycine-like and GABA-like immunoreactivities in Golgi cell terminals in the rat cerebellum: a postembedding light and electron microscopic study , 1988, Brain Research.

[11]  D. Bodznick,et al.  An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish , 1994, Neuroscience Letters.

[12]  N. Spruston,et al.  Action potential initiation and backpropagation in neurons of the mammalian CNS , 1997, Trends in Neurosciences.

[13]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[14]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. II. Intra-axonal recordings show initial stages of central processing. , 1990, Journal of neurophysiology.

[15]  R. Silver,et al.  Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ , 1992, Nature.

[16]  M H Ellisman,et al.  TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  G. Aghajanian,et al.  Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices , 1989, Synapse.

[18]  K. Grant,et al.  Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  C. Bell,et al.  Properties of a modifiable efference copy in an electric fish. , 1982, Journal of neurophysiology.

[20]  K. Grant,et al.  Interneurons of the ganglionic layer in the mormyrid electrosensory lateral line lobe: Morphology, immunohistochemistry, and synaptology , 1996, The Journal of comparative neurology.

[21]  D. Oertel,et al.  Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[23]  P. Manis,et al.  N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus. , 1996, Journal of neurophysiology.

[24]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[25]  Masao Ito.  The Cerebellum And Neural Control , 1984 .

[26]  C. Bell,et al.  Termination of electroreceptor and mechanical lateral line afferents in the mormyrid acousticolateral area , 1978, The Journal of comparative neurology.

[27]  R J Dunn,et al.  N‐methyl‐D‐aspartate receptor 1 mRNA distribution in the central nervous system of the weakly electric fish Apteronotus leptorhynchus , 1997, The Journal of comparative neurology.

[28]  D. Monaghan,et al.  The distribution of excitatory amino acid binding sites in the brain of an electric fish, Apteronotus leptorhynchus , 1991, Journal of Chemical Neuroanatomy.

[29]  David Willshaw,et al.  The cerebellum as a neuronal machine , 1999 .

[30]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: I. Morphology , 1989, The Journal of comparative neurology.

[31]  Mark F. Bear,et al.  Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience , 1995, Nature.

[32]  Bert Sakmann,et al.  Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons , 1995, Neuron.

[33]  A. Konnerth,et al.  Synaptic currents in cerebellar Purkinje cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Masao Ito,et al.  Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex , 1982, Neuroscience Letters.

[35]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[36]  M. Kano,et al.  The glutamate receptor subtype mediating parallel fibre-Purkinje cell transmission in rabbit cerebellar cortex , 1988, Neuroscience Research.

[37]  Paul Antoine Salin,et al.  Cyclic AMP Mediates a Presynaptic Form of LTP at Cerebellar Parallel Fiber Synapses , 1996, Neuron.