Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology

The aim of this study was to determine whether the different morphological classes of pyramidal neurons in layers 2/3 and 5 of rat visual cortex (Larkman and Mason, 1990) have particular electrophysiological properties. Neurons in in vitro slices of rat visual cortex were impaled with glass micropipettes containing horseradish peroxidase (HRP) and studied using current-clamp techniques prior to pressure injection of HRP into the neurons. On morphological grounds, cells stained in layer 2/3 were placed into a single class whereas layer 5 cells were divided into 2 classes. Cells in one of these classes had thick apical dendrites which arborized in layer 1, whereas the apical dendrites of cells in the other class were thinner and did not reach layer 1 (Larkman and Mason, 1990). Despite variation between individual cells of a single class, significant differences were found in the time constants, current/voltage relations, and repetitive firing behaviors of the 3 classes. Burst firing responses to injected current pulses were confined to the layer 5 cells with thick apical dendrites. These results add to those from other areas of the brain demonstrating that the electrophysiological properties of pyramidal neurons are heterogeneous. Furthermore, we have shown that distinctive intrinsic membrane properties of pyramidal neurons in visual cortex are correlated with different morphologies.

[1]  M. Ito,et al.  Electrical behaviour of the motoneurone membrane during intracellularly applied current steps. , 1965, The Journal of physiology.

[2]  D. Kernell High-Frequency Repetitive Firing of Cat Lumbosacral Motoneurones Stimulated by Long-Lasting Injected Currents , 1965 .

[3]  W. Rall Time constants and electrotonic length of membrane cylinders and neurons. , 1969, Biophysical journal.

[4]  P. Schwindt,et al.  Membrane-potential trajectories underlying motoneuron rhythmic firing at high rates. , 1973, Journal of neurophysiology.

[5]  W H Calvin,et al.  Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. , 1976, Journal of neurophysiology.

[6]  D. Prince,et al.  Participation of calcium spikes during intrinsic burst firing in hippocampal neurons , 1978, Brain Research.

[7]  P. Zangger,et al.  Firing behaviour of dorsal spinocerebellar tract neurones. , 1978, The Journal of physiology.

[8]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[9]  M. Descheˆnes,et al.  Morphological characterization of slow and fast pyramidal tract cells in the cat , 1979, Brain Research.

[10]  D. Johnston,et al.  Voltage clamp discloses slow inward current in hippocampal burst-firing neurones , 1980, Nature.

[11]  Kisou Kubota,et al.  Morphological differences between fast and slow pyramidal tract neurons in the monkey motor cortex as revealed by intracellular injection of horseradish peroxidase by pressure , 1981, Neuroscience Letters.

[12]  R K Wong,et al.  Afterpotential generation in hippocampal pyramidal cells. , 1981, Journal of neurophysiology.

[13]  T. Ogawa,et al.  Membrane characteristics of visual cortical neurons in in vitro slices , 1981, Brain Research.

[14]  Paul R. Adams,et al.  Voltage-clamp analysis of muscarinic excitation in hippocampal neurons , 1982, Brain Research.

[15]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[16]  D. A. Brown,et al.  M‐currents and other potassium currents in bullfrog sympathetic neurones , 1982, The Journal of physiology.

[17]  R. Llinás,et al.  Electrophysiology of mammalian thalamic neurones in vitro , 1982, Nature.

[18]  P. Schwindt,et al.  Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro , 1982, Brain Research.

[19]  A. Constanti,et al.  M-current in voltage-clamped olfactory cortex neurones , 1983, Neuroscience Letters.

[20]  M. Mayer,et al.  A voltage‐clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. , 1983, The Journal of physiology.

[21]  J. Parnavelas,et al.  Distribution and morphology of functionally identified neurons in the visual cortex of the rat , 1983, Brain Research.

[22]  P. Schwindt,et al.  Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. , 1984, Journal of neurophysiology.

[23]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[24]  B. Gustafsson,et al.  Relations among passive electrical properties of lumbar alpha‐motoneurones of the cat. , 1984, The Journal of physiology.

[25]  M. Deschenes,et al.  Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. , 1984, Journal of neurophysiology.

[26]  P. Schwindt,et al.  Repetitive firing in layer V neurons from cat neocortex in vitro. , 1984, Journal of neurophysiology.

[27]  P. Schwindt,et al.  Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. , 1985, Journal of neurophysiology.

[28]  J. Munson,et al.  Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. , 1985, Journal of neurophysiology.

[29]  D. McCormick,et al.  Mechanisms of action of acetylcholine in the guinea‐pig cerebral cortex in vitro. , 1986, The Journal of physiology.

[30]  A. Konnerth,et al.  Ionic Properties of Burst Generation in Hippocampal Pyramidal Cell Somata ‘In Vitro’ , 1986 .

[31]  J. V. Halliwell M-current in human neocortical neurones , 1986, Neuroscience Letters.

[32]  B W Connors,et al.  Cellular physiology of the turtle visual cortex: distinctive properties of pyramidal and stellate neurons , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  B. Connors,et al.  Mechanisms of interictal epileptogenesis. , 1986, Advances in neurology.

[34]  J. Hablitz Mechanisms Regulating Synchronization of Hippocampal Epileptiform Activity , 1986 .

[35]  P. Adams,et al.  Voltage-dependent currents of vertebrate neurons and their role in membrane excitability. , 1986, Advances in neurology.

[36]  Alon Friedman,et al.  Synaptic and Intrinsic Mechanisms of Synchronization and Epileptogenesis in the Neocortex , 1986 .

[37]  A. Constanti,et al.  Calcium-dependent action potentials and associated inward currents in guinea-pig neocortical neurons in vitro , 1986, Brain Research.

[38]  F. Crépel,et al.  Inward rectification and low threshold calcium conductance in rat cerebellar Purkinje cells. An in vitro study. , 1986, The Journal of physiology.

[39]  A. Thomson A magnesium‐sensitive post‐synaptic potential in rat cerebral cortex resembles neuronal responses to N‐methylaspartate. , 1986, The Journal of physiology.

[40]  B. Schofield,et al.  Morphology of corticotectal cells in the primary visual cortex of hooded rats , 1987, The Journal of comparative neurology.

[41]  A. Friedman,et al.  Low-threshold calcium electrogenesis in neocortical neurons , 1987, Neuroscience Letters.

[42]  S. A. Shefner,et al.  Anomalous rectification in rat locus coeruleus neurons , 1987, Brain Research.

[43]  R. Calabrese,et al.  Ionic conductances underlying the activity of interneurons that control heartbeat in the medicinal leech , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  H. Scharfman,et al.  Responses to GABA recorded from identified rat visual cortical neurons , 1987, Neuroscience.

[45]  Etienne Audinat,et al.  Excitation of rat prefrontal cortical neurons by dopamine: An in vitro electrophysiological study , 1987, Brain Research.

[46]  R Llinás,et al.  Long-term modifiability of anomalous and delayed rectification in guinea pig inferior olivary neurons , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  D. Prince,et al.  Effect of D890 on membrane properties of neocortical neurons , 1987, Brain Research.

[48]  P. Schwindt,et al.  Anomalous rectification in neurons from cat sensorimotor cortex in vitro. , 1987, Journal of neurophysiology.

[49]  C. Koch,et al.  The dynamics of free calcium in dendritic spines in response to repetitive synaptic input. , 1987, Science.

[50]  D. McCormick,et al.  Post‐natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. , 1987, The Journal of physiology.

[51]  W. Singer,et al.  Long-term potentiation and NMDA receptors in rat visual cortex , 1987, Nature.

[52]  A. Peters Number of Neurons and Synapses in Primary Visual Cortex , 1987 .

[53]  D. McCormick,et al.  Noradrenergic modulation of firing pattern in guinea pig and cat thalamic neurons, in vitro. , 1988, Journal of neurophysiology.

[54]  I Segev,et al.  Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. , 1988, Journal of neurophysiology.

[55]  Johan F. Storm,et al.  Temporal integration by a slowly inactivating K+ current in hippocampal neurons , 1988, Nature.

[56]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.

[57]  P. Schwindt,et al.  Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. , 1988, Journal of neurophysiology.

[58]  P. Schwindt,et al.  Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. , 1988, Journal of neurophysiology.

[59]  W. Griffith,et al.  Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. , 1988, Journal of neurophysiology.

[60]  C. Blakemore,et al.  The in vitro slice preparation for combined morphological and electrophysiological studies of rat visual cortex , 1988, Neuroscience Research.

[61]  Nonequivalent cylinder models of neurons: interpretation of voltage transients generated by somatic current injection. , 1988, Journal of neurophysiology.

[62]  E M Lasater,et al.  Membrane currents of retinal bipolar cells in culture. , 1988, Journal of neurophysiology.

[63]  J. López-Barneo,et al.  Differential burst firing modes in neurons of the mammalian visual cortex in vitro , 1988, Brain Research.

[64]  J T Williams,et al.  Voltage- and ligand-activated inwardly rectifying currents in dorsal raphe neurons in vitro , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  R. S. Jones,et al.  Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. , 1988, Journal of neurophysiology.

[66]  J. Hounsgaard,et al.  Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro. , 1988, The Journal of physiology.

[67]  Repetitive firing properties of phrenic motoneurons in the cat. , 1988, Journal of neurophysiology.

[68]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

[69]  P. Schwindt,et al.  Influence of anomalous rectifier activation on afterhyperpolarizations of neurons from cat sensorimotor cortex in vitro. , 1988, Journal of neurophysiology.

[70]  M. Avoli,et al.  Delayed and fast transient potassium currents in rat neocortical neurons in cell culture , 1988, Neuroscience Letters.

[71]  R Llinás,et al.  Electrophysiology of mammalian tectal neurons in vitro. I. Transient ionic conductances. , 1988, Journal of neurophysiology.

[72]  Effect of subthreshold voltage-dependent conductances on the transfer function of branched excitable cells and the conduction of synaptic potentials. , 1988, Journal of neurophysiology.

[73]  Michael W. Miller Maturation of rat visual cortex: IV. The generation, migration, morphogenesis, and connectivity of atypically oriented pyramidal neurons , 1988, The Journal of comparative neurology.

[74]  Differences in somatic and dendritic specific membrane resistivity of spinal motoneurons: an electrophysiological study of neck and shoulder motoneurons in the cat. , 1988, Journal of neurophysiology.

[75]  A. Thomson,et al.  Voltage-dependent currents prolong single-axon postsynaptic potentials in layer III pyramidal neurons in rat neocortical slices. , 1988, Journal of neurophysiology.

[76]  A. Friedman,et al.  Intracellular Calcium and Control of Burst Generation in Neurons of Guinea‐Pig Neocortex in Vitro , 1989, The European journal of neuroscience.

[77]  A Olivier,et al.  Electrophysiological properties and synaptic responses in the deep layers of the human epileptogenic neocortex in vitro. , 1989, Journal of neurophysiology.

[78]  P. Schwindt,et al.  Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. , 1989, Journal of neurophysiology.

[79]  P. Schwindt,et al.  Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons. , 1989, Journal of neurophysiology.

[80]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.