Suprathreshold excitation of frog tectal neurons by short spike trains of single retinal ganglion cell

It has been established that coincident inputs from multiple presynaptic axons are required to achieve a suprathreshold level of excitation for the most of central neurons. The present study, however, was designed to determine whether a train of spikes of an individual retinal ganglion cell (that is, input from a single presynaptic axon) targeting a frog tectum layer F could evoke suprathreshold excitation of tectal neurons. The lungs of immobilized frog were artificially ventilated during experiments. An individual ganglion cell was electrically stimulated in the retina through a multi-channel electrode. Responses evoked in the tectum by the stimulation were recorded extracellularly from a terminal arborization of the retinotectal fiber using the carbon-fiber microelectrode. Negative and negative-positive spikes (referred to as first type population responses) and polyphasic spikes followed by excitatory synaptic potentials (referred to as second type population responses) were observed in the recordings of retinotectal activity. Usually, the population responses have ensued after the frequency facilitated first and/or second testing individual retinotectal synaptic potential and disappeared in a threshold manner with a reduction of retinotectal transmission by an application of kynurenic acid. These observations have suggested that the population responses were a consequence of a suprathreshold excitation of tectal neurons and, therefore, could serve as the sign for such an excitation. Recordings have also demonstrated that sources of the first type population responses (likely, the hillocks of axons or somas of postsynaptic neurons) lie deeper than the optic fiber layer F of the tectum, whereas sources of the second type population responses (likely, axon terminal arborizations of these postsynaptic neurons) are scattered throughout the optic fiber layers. The findings have suggested: 1) a short train of action potentials of an individual retinal ganglion cell (likely darkness, also known as 5th, detector) can excite tectal neurons to suprathreshold level; 2) tectal and perhaps, nucleus isthmi neurons that make up recurrent connection circuits to the optic fiber layers of the tectum are also activated; 3) a suprathreshold level for an individual retinotectal input is achieved primarily due to the frequency facilitation of synaptic potentials; and 4) an artificial ventilation of the lungs of immobilized frog favors the eliciting of a suprathreshold excitation of tectal neurons, demonstrating that the ventilation certainly improves the physiological condition of a frog.

[1]  H. D. Potter Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana) , 1969, The Journal of comparative neurology.

[2]  G. Székely,et al.  Tectal neurons of the frog: Intracellular recording and labeling with cobalt electrodes , 1986, The Journal of comparative neurology.

[3]  H. Lüscher,et al.  Effects of impulse frequency, PTP, and temperature on responses elicited in large populations of motoneurons by impulses in single Ia-fibers. , 1983, Journal of neurophysiology.

[4]  B Sakmann,et al.  Postsynaptic Ca2+ Influx Mediated by Three Different Pathways during Synaptic Transmission at a Calyx-Type Synapse , 1998, The Journal of Neuroscience.

[5]  J. Ewert,et al.  Thalamus, Praetectum, Tectum: Retinale Topographie und physiologische Interaktionen bei der KröteBufo bufo (L.) , 1974, Journal of comparative physiology.

[6]  H. Mitsuda,et al.  Effects of a high concentration of CO2 on electrocardiograms in the carp, Cyprinus carpio. , 1988, Comparative biochemistry and physiology. A, Comparative physiology.

[7]  D. Jackson,et al.  Respiratory control in bullfrogs: Cutaneous versus pulmonary response to selective CO2 exposure , 1979, Journal of Comparative Physiology.

[8]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  James G. King,et al.  Selective, unilateral, reversible loss of behavioral responses to looming stimuli after injection of tetrodotoxin or cadmium chloride into the frog optic nerve , 1999, Brain Research.

[10]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[11]  Antanas Kuras,et al.  Multi-channel metallic electrode for threshold stimulation of frog's retina , 1997, Journal of Neuroscience Methods.

[12]  T. Hughes A light- and electron-microscopic investigation of the optic tectum of the frog, Rana pipiens, I: The retinal axons , 1990, Visual Neuroscience.

[13]  R. B. Langdon,et al.  Pharmacology of retinotectal transmission in the goldfish: effects of nicotinic ligands, strychnine, and kynurenic acid , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  A. Mendonça,et al.  Presynaptic inhibitory receptors mediate the depression of synaptic transmission upon hypoxia in rat hippocampal slices , 2000, Brain Research.

[15]  W. Pitts,et al.  Anatomy and Physiology of Vision in the Frog (Rana pipiens) , 1960, The Journal of general physiology.

[16]  H. Stødkilde-Jørgensen,et al.  CO2 induced acute respiratory acidosis and brain tissue intracellular pH: a 31P NMR study in swine , 2003, Laboratory animals.

[17]  R. Miles,et al.  Excitatory synaptic interactions between CA3 neurones in the guinea‐pig hippocampus. , 1986, The Journal of physiology.

[18]  A. Kuras,et al.  N-cholinergic facilitation of glutamate release from an individual retinotectal fiber in frog , 2001, Visual Neuroscience.

[19]  D Debanne,et al.  Physiology and pharmacology of unitary synaptic connections between pairs of cells in areas CA3 and CA1 of rat hippocampal slice cultures. , 1995, Journal of neurophysiology.

[20]  P. Somogyi,et al.  Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. , 1997, The Journal of physiology.

[21]  M. Ferragamo,et al.  Octopus cells of the mammalian ventral cochlear nucleus sense the rate of depolarization. , 2002, Journal of neurophysiology.

[22]  J. Guinan,et al.  Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat , 1990, Hearing Research.

[23]  G. Székely,et al.  Fine structure of the frog's optic tectum: optic fibre termination layers. , 1973, Journal fur Hirnforschung.

[24]  A. Thomson,et al.  Facilitating pyramid to horizontal oriens‐alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus , 1998, The Journal of physiology.

[25]  A. Kuras,et al.  Preparation of carbon-fibre microelectrode for extracellular recording of synaptic potentials , 1995, Journal of Neuroscience Methods.

[26]  S. Udin,et al.  Topographic projections between the nucleus isthmi and the tectum of the frog rana pipiens , 1978, The Journal of comparative neurology.

[27]  J. Kwak,et al.  Effect of hypoxia on excitatory transmission in the rat substantia gelatinosa neurons. , 2002, Biochemical and biophysical research communications.

[28]  B. Sakmann,et al.  Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. , 1992, The Journal of physiology.

[29]  G. Székely,et al.  Golgi studies on the optic center of the frog. , 1967, Journal fur Hirnforschung.

[30]  H. D. Potter Terminal arborizations of retinotectal axons in the bullfrog , 1972, The Journal of comparative neurology.

[31]  P. Schwindt,et al.  Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. , 1999, Journal of neurophysiology.

[32]  B. Sakmann,et al.  Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex , 1999, Nature Neuroscience.

[33]  O Kiehn,et al.  Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle motoneurones in vitro. , 1993, The Journal of physiology.

[34]  H. Nakagawa,et al.  Principal neuronal organization in the frog optic tectum revealed by a current source density analysis , 1997, Visual Neuroscience.

[35]  E. V. Deusen,et al.  Pharmacologic evidence for NMDA, APB and kainate/quisqualate retinotectal transmission in the isolated whole tectum of goldfish , 1990, Brain Research.

[36]  D. Ingvar,et al.  Carbon dioxide narcosis: influence of short-term high concentration carbon dioxide inhalation on EEG and cortical evoked responses in the rat. , 1986, Acta physiologica Scandinavica.

[37]  A. Gutman,et al.  Effects of cadmium ions on synaptic transmission in the frog tectum , 2005, Neurophysiology.

[38]  M. C. Angulo,et al.  Postsynaptic glutamate receptors and integrative properties of fast-spiking interneurons in the rat neocortex. , 1999, Journal of neurophysiology.

[39]  R. Silver,et al.  Synaptic connections between layer 4 spiny neurone‐ layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column , 2002, The Journal of physiology.

[40]  W. C. Groat,et al.  Unitary excitatory synaptic currents in preganglionic neurons mediated by two distinct groups of interneurons in neonatal rat sacral parasympathetic nucleus. , 1996, Journal of neurophysiology.

[41]  S. Udin,et al.  Latency and temporal overlap of visually elicited contralateral and ipsilateral firing in Xenopus tectum during and after the critical period. , 1991, Brain research. Developmental brain research.

[42]  D. Seol,et al.  Regulation of Akt by EGF-R inhibitors, a possible mechanism of EGF-R inhibitor-enhanced TRAIL-induced apoptosis. , 2002, Biochemical and biophysical research communications.

[43]  W. B. Marks,et al.  Optic nerve terminal arborizations in the frog: shape and orientation inferred from electrophysiological measurements. , 1974, Experimental neurology.