Feature Article a Brief History of Time (constants)

That the cerebral cortex processes information at prodigious speeds cannot be doubted. Yet the passive time constant •*„ of neurons, often thought of as a measure of the neuron's "response time" to synaptic input is relatively long. In the 1950s, T O was estimated to be only a few milliseconds for mammalian central neurons; with improvement in recording techniques, its estimated value grew over the years and it now stands near 20-100 msec. However, as we will argue here, the functional meaning of tm is ambiguous. On the basis of a newly introduced definition of local delay, we show that the time window for synaptic integration in passive dendritic trees can be much smaller than the time constant We argue that the voltage response to very brief synaptic inputs is essentially independent of •:„ We discuss how ta can change dynamically with the global activity of the network, as well as the difficulties of defining a time constant in structures with voltage-dependent elements. We conclude that the classically defined Ta only provides a very rough estimate, typically an overestimate, of the response time of neurons and that alternative measures are required to capture the dependency of the time course of the membrane potential on ligand-gated and/or voltage-dependent membrane conductances.

[1]  Idan Segev,et al.  The Impact of Parallel Fiber Background Activity on the Cable Properties of Cerebellar Purkinje Cells , 1992, Neural Computation.

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

[3]  T. Poggio,et al.  Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[4]  F. A. Edwards,et al.  A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system , 1989, Pflügers Archiv.

[5]  Masakazu Konishi,et al.  Deciphering the Brain's Codes , 1999, Neural Computation.

[6]  J. Eccles,et al.  The recording of potentials from motoneurones with an intracellular electrode , 1952, The Journal of physiology.

[7]  William Albert Hugh Rushton,et al.  Initiation of the Propagated Disturbance , 1937 .

[8]  A. Reyes,et al.  Membrane properties underlying the firing of neurons in the avian cochlear nucleus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  T. H. Brown,et al.  Passive electrical constants in three classes of hippocampal neurons. , 1981, Journal of neurophysiology.

[10]  Electrical activity of single spinal cord elements. , 1952, Cold Spring Harbor symposia on quantitative biology.

[11]  H. Hirsch,et al.  Receptive-field properties of neurons in different laminae of visual cortex of the cat. , 1978, Journal of neurophysiology.

[12]  I Segev,et al.  Signal delay and input synchronization in passive dendritic structures. , 1993, Journal of neurophysiology.

[13]  Y Yarom,et al.  Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. , 1990, Journal of neurophysiology.

[14]  B. Sakmann,et al.  Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. , 1993, The Journal of physiology.

[15]  Walter Heiligenberg,et al.  Temporal hyperacuity in the electric sense of fish , 1985, Nature.

[16]  L. Cauller,et al.  Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  W. Rall Membrane time constant of motoneurons. , 1957, Science.

[18]  C. Nicholson Electric current flow in excitable cells J. J. B. Jack, D. Noble &R. W. Tsien Clarendon Press, Oxford (1975). 502 pp., £18.00 , 1976, Neuroscience.

[19]  M. Konishi,et al.  Neuronal and behavioral sensitivity to binaural time differences in the owl , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  D. Whitteridge,et al.  An intracellular analysis of the visual responses of neurones in cat visual cortex. , 1991, The Journal of physiology.

[21]  William R. Softky,et al.  Sub-millisecond coincidence detection in active dendritic trees , 1994, Neuroscience.

[22]  J Rinzel,et al.  Transient response in a dendritic neuron model for current injected at one branch. , 1974, Biophysical journal.

[23]  Y Yarom,et al.  Physiology, morphology and detailed passive models of guinea‐pig cerebellar Purkinje cells. , 1994, The Journal of physiology.

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

[25]  A. Hodgkin,et al.  The electrical constants of a crustacean nerve fibre , 1946, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[26]  Idan Segev,et al.  The theoretical foundation of dendritic function: Selected papers of Wilfrid Rall with commentaries , 1994 .

[27]  Idan Segev,et al.  Subthreshold oscillations and resonant frequency in guinea‐pig cortical neurons: physiology and modelling. , 1995, The Journal of physiology.

[28]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[29]  C. Stevens,et al.  Inward and delayed outward membrane currents in isolated neural somata under voltage clamp , 1971, The Journal of physiology.

[30]  Daniel J Amittt Effective neurons and attractor neural networks in cortical environment , 1992 .

[31]  N. Spruston,et al.  Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. , 1992, Journal of neurophysiology.

[32]  R W GERARD,et al.  Membrane potentials and excitation of impaled single muscle fibers. , 1946, Journal of cellular and comparative physiology.

[33]  Patton Hd,et al.  Electrical activity of single spinal cord elements. , 1952 .

[34]  B Sakmann,et al.  Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  M Konishi,et al.  The owl's cochlear nuclei process different sound localization cues. , 1985, The Journal of the Acoustical Society of America.

[36]  J. Eccles,et al.  The electrical properties of the motoneurone membrane , 1955, The Journal of physiology.

[37]  J. C. Anderson,et al.  Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex , 1994, The Journal of comparative neurology.

[38]  W Rall,et al.  Interpretation of time constant and electrotonic length estimates in multicylinder or branched neuronal structures. , 1992, Journal of neurophysiology.

[39]  Shaul Hestrin,et al.  Activation and desensitization of glutamate-activated channels mediating fast excitatory synaptic currents in the visual cortex , 1992, Neuron.

[40]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  A. Hodgkin,et al.  A surprising property of electrical spread in the network of rods in the turtle's retina , 1978, Nature.

[42]  T. Poggio,et al.  A theoretical analysis of electrical properties of spines , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[43]  Daniel Johnston,et al.  Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties , 1994, Trends in Neurosciences.

[44]  W Rall,et al.  Computational study of an excitable dendritic spine. , 1988, Journal of neurophysiology.

[45]  PlvricsDepartment,et al.  Realistic synaptic inputs for model neural networks , .

[46]  L. Trussell,et al.  Desensitization of AMPA receptors upon multiquantal neurotransmitter release , 1993, Neuron.

[47]  J. Clements,et al.  Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. , 1989, The Journal of physiology.

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

[49]  H. Markram,et al.  Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Nicoll,et al.  Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices , 1990, Neuron.

[51]  R. Benz,et al.  Electrical capacity of black lipid films and of lipid bilayers made from monolayers. , 1975, Biochimica et biophysica acta.

[52]  A. Larkman,et al.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions , 1991, The Journal of comparative neurology.

[53]  Connor Ja,et al.  Slow repetitive activity from fast conductance changes in neurons. , 1978 .

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

[55]  C. Koch,et al.  A brief history of time (constants). , 1996, Cerebral cortex.

[56]  L. J. Bindman,et al.  Comparison of the electrical properties of neocortical neurones in slices in vitro and in the anaesthetized rat , 2004, Experimental Brain Research.

[57]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[58]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  C. Stevens,et al.  Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma , 1971, The Journal of physiology.

[60]  P Andersen,et al.  Excitatory synaptic integration in hippocampal pyramids and dentate granule cells. , 1990, Cold Spring Harbor symposia on quantitative biology.

[61]  Intradendritic recordings from neurons of motor cortex of cats. , 1984, Journal of neurophysiology.

[62]  C. Koch,et al.  Synaptic background activity influences spatiotemporal integration in single pyramidal cells. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Marius Usher,et al.  The Effect of Synchronized Inputs at the Single Neuron Level , 1994, Neural Computation.

[64]  Idan Segev,et al.  Synaptic integration mechanisms. Theoretical and experimental investigation of temporal postsynaptic interactions between excitatory and inhibitory inputs. , 1983, Biophysical journal.

[65]  Idan Segev,et al.  The morphoelectrotonic transform: a graphical approach to dendritic function , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  J J Jack,et al.  Solutions for transients in arbitrarily branching cables: I. Voltage recording with a somatic shunt. , 1993, Biophysical journal.

[67]  R. Burke,et al.  Electrotonic characteristics of alpha motoneurones of varying size , 1971, The Journal of physiology.