Rate coding and spike-time variability in cortical neurons with two types of threshold dynamics

Journal of Neurophysiology

Volumn 95, Issue 4, 2006, Pages 2650-2663

  Tateno, T ^a,b,c   Robinson, H P C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

^c NONE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROSTIMULATION; INTERNEURON; NERVE CONDUCTION; NEUROPHYSIOLOGY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RELIABILITY; SOMATOSENSORY CORTEX; SPIKE; STIMULUS RESPONSE; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; ANIMALS; EVOKED POTENTIALS, SOMATOSENSORY; EXCITATORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; NEURAL CONDUCTION; NEURAL INHIBITION; NEURONS, AFFERENT; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, GABA-A; SENSORY THRESHOLDS; SOMATOSENSORY CORTEX; SYNAPSES; TIME FACTORS;

EID: 33646191839     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00683.2005     Document Type: Article

References (61)

1. Azouz R and Gray CM. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209-2223, 1999.
2. Beierlein M, Gibson JR, and Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904-910, 2000.
3. Beierlein M, Gibson JR, and Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003.
4. Britten KH, Shadlen MN, Newsome WT, and Movshon JA. Responses of neurons in macaque MT to stochastic motion signals. Vis Neurosci 10: 1157-1169, 1993.
5. Bryant HL and Segundo JP. Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260: 279-314, 1976.
6. Buracas GT, Zador AM, DeWeese MR, and Albright TD. Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20: 959-969, 1998.
7. Chance FS, Abbott LF, and Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
8. Connors BW and Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99-104, 1990.
9. Connors BW, Gutnick MJ, and Prince DA. Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48: 1302-1320, 1982.
10. Connors BW, Malenka RC, and Silva LR. Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J Physiol 406: 443-468, 1988.
11. de Polavieja GG, Harsch A, Kleppe I, Robinson HPC, and Juusola M. Stimulus history reliably shapes action potential waveforms of cortical neurons. J Neurosci 25: 5657-5665, 2005.
12. Destexhe A, Rudolph M, and Paré D. The high-conductance state of neocortical neurons in vivo. Nature Rev Neurosci 4: 739-751, 2003.
13. Edwards FA, Konnerth A, and Sakmann B. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J Physiol 430: 213-249, 1990.
14. Erisir A, Lau D, Rudy B, and Leonard CS. Function of specific K channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82: 2476-2489, 1999.
15. Ermentrout B. Type 1 membrane, phase resetting curves, and synchrony. Neural Comp 8: 979-1002, 1996.
16. Galarreta M and Hestrin S. Spike transmission and synchrony detection in networks of GABAergic interneurons, Science 292: 2295-2299, 2001.
17. Gershon ED, Wiener MC, Latham PE, and Richmond BJ. Coding strategies in monkey V1 and inferior temporal cortices. J Neurophysiol 79: 1135-1144, 1998.
18. Gibson JR, Beierlin M, and Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex, Nature 402: 75-79, 1999.
19. Gutkin B and Ermentrout B. Dynamics of membrane excitability determine interspike interval variability: a link between spike generation and cortical spike train statistics. Neural Comput 10: 1047-1065, 1998.
20. Gutkin B, Ermentrout GB, and Rudolph M. Spike generating dynamics and the conditions for spike-time precision in cortical neurons. J Comput Neurosci 15: 91-103, 2003.
21. Harsch A and Robinson HPC. Postsynaptic variability of firing in rat cortical neurons: the roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20: 6181-6192, 2000.
22. Häusser M and Clark BA. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19: 665-678, 1997.
23. Häusser M and Roth A. Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method. J Neurosci 17: 7606-7625, 1997.
24. Hestrin S. Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron 11: 1083-1091, 1993.
25. Hodgkin AL. The local electric changes associated with repetitive action in a non-medullated axon. J Physiol 107: 165-181, 1948.
26. Hollmann M and Heinemann S. Cloned Glutamate Receptors. Annu Rev Neurosci 17: 31-108, 1994.
27. Kapur A, Pearce RA, Lytton WW, and Haberly LB. GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J Neurophysiol 78: 2531-2545, 1997.
28. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15: 2638-2655, 1995.
29. Kawaguchi Y and Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476-486, 1997.
30. Kleppe IC and Robinson HP. Determining the activation time course of synaptic AMPA receptors from openings of colocalized NMDA receptors. Biophys J 77: 1418-1427, 1999.
31. Koch C. Biophysics of Computation: Information Processing in Single Neurons. New York: Oxford Univ. Press, 1999, p. 85-116.
32. Krahe R and Gabbiani F. Burst firing in sensory systems. Nat Rev Neurosci 5: 13-23, 2004.
33. Ling DS and Benardo LS. Restrictions on inhibitory circuits contribute to limited recruitment of fast inhibition in rat neocortical pyramidal cells. J Neurophysiol 82: 1793-1807, 1999.
34. MacDermott AB and Dale N. Receptors, ion channels and synaptic potentials underlying the integrative actions of excitatory amino acids. Trends Neurosci 87: 280-284, 1987.
35. Mainen ZF and Sejnowski TJ. Reliability of spike timing in neocortical neurons. Science 268: 1503-1506, 1995.
36. Mitchell SJ and Silver RA. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38: 433-445, 2003.
37. Morris C and Lecar H. Voltage oscillations in the barnacle giant muscle fibre. Biophys J 35: 193-213, 1981.
38. Nowak LG, Sanchez-Vives MV, and McCormick DA. Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb Cortex 7: 487-501, 1997.
39. Pearce RA. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10: 189-200, 1993.
40. Rinzel J and Ermentrout B. Analysis of neural excitability and oscillations. In: Methods in Neuronal Modelling: From Ions to Networks, edited by Koch C and Segev I. Cambridge, MA: MIT Press, 1998, p. 251-291.
41. Robinson HPC and Harsch A. Stages of spike time variability during neuronal responses to transient inputs. Phys Rev E 66: 061902, 2002.
42. Robinson HPC and Kawai N. Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49: 157-165, 1993.
43. Robinson HPC. The biophysical basis of firing variability in cortical neurons. In: Computational Neuroscience: A Comprehensive Approach, edited by Feng JF. London: CRC LLC, 2004, p. 159-183.
44. Sacchi O, Rossi ML, Canella R, and Fesce R. Synaptic current at the rat ganglionic synapse and its interactions with the neuronal voltage-dependent currents. J Neurophysiol 79: 727-742, 1998.
45. Sakmann B and Stuart G. Patch-pipette recordings from the soma, dendrites and axon of neurons in brain slices. In: Single-Channel Recording, edited by Sakmann B and Neher E. New York: Plenum Press, 1995, p. 199-211.
46. Salin PA and Prince DA. Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol 75: 1573-1588, 1996.
47. Shadlen MN and Newsome WT. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 15: 3870-3896, 1998.
48. Sharp AA, O'Neil MB, Abbott LF, and Marder E. Dynamic clamp: computer-generated conductances in real neurons. J Neurophysiol 69: 992-995, 1993.
49. Snowden RJ, Treue S, and Andersen RA. The response of neurons in areas V1 and MT of the alert rhesus monkey to moving random dot patterns. Exp Brain Res 88: 389-400, 1992.
50. Softky WR and Koch C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334-350, 1993.
51. Stern P, Edwards FA, and Sakmann B. Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. J Physiol 449: 247-278, 1992.
52. Stevens CF and Zador AM. Input synchrony and the irregular firing of cortical neurons. Nat Neurosci 1: 210-217, 1998.
53. Suter KJ and Jaeger D. Reliable control of spike rate and spike timing by rapid input transits in cerebellar stellate cells. Neuroscience 124: 305-317, 2004.
54. Tang AC, Bartels AM, and Sejnowski TJ. Effects of cholinergic modulation on responses of neocortical neurons to fluctuating input. Cereb Cortex 7: 502-509, 1997.
55. Tateno T, Harsch A, and Robinson HPC. Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. J Neurophysiol 92: 2283-2299, 2004.
56. Tateno T, Kawana A, and Jimbo Y. Analytical characterization of spontaneous firing in networks of developing rat cultured cortical neurons. Phys Rev E 65: 051924, 2002.
57. Tolhurst DJ, Movshon JA, and Dean AF. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23: 775-785, 1983.
58. Tomko GT and Crapper DR. Neuronal variability: non-stationary responses to identical visual stimuli. Brain Res 79: 405-418, 1974.
59. Turcott RG, Lowen SB, Li E, Johnson DH, Tsuchitani C, and Teich MC. A nonstationary Poisson point process describes the sequence of action potentials over long time scales in lateral-superior-olive auditory neurons. Biol Cybern 70: 209-217, 1994.
60. Tsodyks M, Kenet T, Grinvald A, and Arieli A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286: 1943-1946, 1999.
61. Wehr M and Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446, 2003.