Factors determining the precision of the correlated firing generated by a monosynaptic connection in the cat visual pathway

Journal of Physiology

Volumn 567, Issue 3, 2005, Pages 1057-1078

  Veredas, Francisco J ^a   Vico, Francisco J ^a   Alonso, Jose Manuel ^b,c  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; AMPLITUDE MODULATION; CAT; COMPARTMENT MODEL; CONTROLLED STUDY; CORRELATION ANALYSIS; EXCITATORY POSTSYNAPTIC POTENTIAL; LATENT PERIOD; MATHEMATICAL COMPUTING; MONOSYNAPTIC REFLEX; NONHUMAN; POLYSYNAPTIC REFLEX; PRESYNAPTIC NERVE; PRIORITY JOURNAL; REVIEW; SENSORY NERVE CONDUCTION; SIGNAL NOISE RATIO; SIMULATION; THALAMUS; TIME; VISUAL CORTEX; VISUAL SYSTEM; ACTION POTENTIAL; ACTION POTENTIAL AMPLITUDE; ANIMAL CELL; ARTICLE; CELL MEMBRANE CONDUCTANCE; CORTICOCORTICAL CONNECTION; FIRING RATE; GENICULOCORTICAL CONNECTION; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; POLYSYNAPTIC INPUT; RETINOGENICULATE CONNECTION; REVERSAL POTENTIAL; VISUAL THRESHOLD;

ANIMALS; CATS; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; NEURONS; SYNAPTIC TRANSMISSION; VISUAL PATHWAYS;

EID: 25844518608     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.092882     Document Type: Review

References (99)

1. Aertsen AM, Gerstein GL, Habib MK & Palm G (1989). Dynamics of neuronal firing correlation: modulation of 'effective connectivity: J Neurophysiol 61, 900-917.
2. Alonso JM & Martinez LM (1998). Functional connectivity between simple cells and complex cells in cat striate cortex. Nat Neurosci 1, 395-403.
3. Alonso JM, Usrey WM & Reid RC (1996). Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815-819.
4. Alonso JM, Usrey WM & Reid RC (2001). Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. J Neurosci 21, 4002-4015.
5. Andreasen M & Lambert JD (1999). Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurones. J Physiol 519, 85-100.
6. Axmacher N & Miles R (2004). Intrinsic cellular currents and the temporal precision of EPSP-action potential coupling in CA1 pyramidal cells. J Physiol 555, 713-725.
7. Azouz R & Gray CM (2000). Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc Natl Acad Sci U S A 97, 8110-8115.
8. Azouz R & Gray CM (2003). Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37, 513-523.
9. Bell CC, Han VZ, Sugawara Y & Grant K (1997). Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387, 278-281.
10. Bi GQ & Poo MM (1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18, 10464-10472.
11. Bienenstock EL, Cooper LN & Munro PW (1982). Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2, 32-48.
12. Bloomfield SA & Sherman SM (1988). Postsynaptic potentials recorded in neurons of the cat's lateral geniculate nucleus following electrical stimulation of the optic chiasm. J Neurophysiol 60, 1924-1945.
13. Brody CD (1998). Slow covariations in neuronal resting potentials can lead to artefactually fast cross-correlations in their spike trains. J Neurophysiol 80, 3345-3351.
14. Chen C & Regehr WG (2000). Developmental remodeling of the retinogeniculate synapse. Neuron 28, 955-966.
15. Cleland BG, Dubin MW & Levick WR (1971a). Simultaneous recording of input and output of lateral geniculate neurones. Nat New Biol 231, 191-192.
16. Cleland BG, Dubin MW & Levick WR (1971b). Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J Physiol 217, 473-496.
17. Cope TC, Fetz EE & Matsumura M (1987). Cross-correlation assessment of synaptic strength of single Ia fibre connections with triceps surae motoneurones in cats. J Physiol 390, 161-188.
18. Creutzfeldt O, Hellweg FC & Schreiner C (1980). Thalamocortical transformation of responses to complex auditory stimuli. Exp Brain Res 39, 87-104.
19. Debanne D, Gahwiler BH & Thompson SM (1998). Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol 507, 237-247.
20. Diesmann M, Gewaltig MO & Aertsen A (1999). Stable propagation of synchronous spiking in cortical neural networks. Nature 402, 529-533.
21. Dorn JD & Ringach DL (2003). Estimating membrane voltage correlations from extracellular spike trains. J Neurophysiol 89, 2271-2278.
22. Eggermont JJ, Smith GM & Bowman D (1993). Spontaneous burst firing in cat primary auditory cortex: age and depth dependence and its effect on neural interaction measures. J Neurophysiol 69, 1292-1313.
23. Eysel UT (1976). Quantitative studies of intracellular postsynaptic potentials in the lateral geniculate nucleus of the cat with respect to optic tract stimulus response latencies. Exp Brain Res 25, 469-486.
24. Feldmeyer D, Lubke J, Silver RA & Sakmann B (2002). 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. J Physiol 538, 803-822.
25. Feldmeyer D, Roth A & Sakmann B (2005). Monosynaptic connections between pairs of spiny stellate cells in layer 4 and pyramidal cells in layer 5A indicate that lemniscal and paralemniscal afferent pathways converge in the infragranular somatosensory cortex. J Neurosci 25, 3423-3431.
26. Feldmeyer D & Sakmann B (2000). Synaptic efficacy and reliability of excitatory connections between the principal neurones of the input (layer 4) and output layer (layer 5) of the neocortex. J Physiol 525, 31-39.
27. Ferster D & Lindstrom S (1983). An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. J Physiol 342, 181-215.
28. Fetz EE & Gustafsson B (1983). Relation between shapes of post-synaptic potentials and changes in firing probability of cat motoneurones. J Physiol 341, 387-410.
29. FitzHugh R (1961). Impulses and physiological states in theoretical models of nerve membranes. Biophysical Journal 1, 445-466.
30. Freund TF, Martin KA, Somogyi P & Whitteridge D (1985). Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y-type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation. J Comp Neurol 242, 275-291.
31. Fricker D & Miles R (2000). EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28, 559-569.
32. Friedlander MJ, Lin CS & Sherman SM (1979). Structure of physiologically identified X and Y cells in the cat's lateral geniculate nucleus. Science 204, 1114-1117.
33. Froemke RC & Dan Y (2002). Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416, 433-438.
34. Fu YX, Djupsund K, Gao H, Hayden B, Shen K & Dan Y (2002). Temporal specificity in the cortical plasticity of visual space representation. Science 296, 1999-2003.
35. Galarreta M & Hestrin S (1999). A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72-75.
36. Galarreta M & Hestrin S (2001). Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292, 2295-2299.
37. Gerstein GL & Aertsen AM (1985). Representation of cooperative firing activity among simultaneously recorded neurons. J Neurophysiol 54, 1513-1528.
38. Gerstein GL & Perkel DH (1972). Mutual temporal relationships among neuronal spike trains. Statistical techniques for display and analysis. Biophys J 12, 453-473.
39. Gerstein GL, Perkel DH & Dayhoff JE (1985). Cooperative firing activity in simultaneously recorded populations of neurons: detection and measurement. J Neurosci 5, 881-889.
40. Gibson JR, Beierlein M & Connors BW (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79.
41. Gray CM, Engel AK, Konig P & Singer W (1990). Stimulus-dependent neuronal oscillations in cat visual cortex: receptive field properties and feature dependence. Eur J Neurosci 2, 607-619.
42. Gustafsson B & McCrea D (1984). Influence of stretch-evoked synaptic potentials on firing probability of cat spinal motoneurones. J Physiol 347, 431-451.
43. Hamos JE, Van Horn SC, Raczkowski D & Sherman SM (1987). Synaptic circuits involving an individual retinogeniculate axon in the cat. J Comp Neurol 259, 165-192.
44. Hirsch JA, Alonso JM, Reid RC & Martinez LM (1998). Synaptic integration in striate cortical simple cells. J Neurosci 18, 9517-9528.
45. Hodgkin AL & Huxley AF (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117, 500-544.
46. Hubel DH & Wiesel TN (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160, 106-154.
47. Jack JB, Noble D & Tsien RW (1983). Electric Current Flow in Excitable Cells. Oxford University Press, Oxford.
48. Kara P & Reid RC (1999). Efficacy of disynaptic retinal inputs to visual cortex. Soc for Neuroscience Abstracts 25, 277.
49. Kara P, Reinagel P & Reid RC (2000). Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27, 635-646.
50. Katz LC & Shatz CJ (1996). Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138.
51. Kirkwood PA (1979). On the use and interpretation of cross-correlations measurements in the mammalian central nervous system. J Neurosci Meth 1, 107-132.
52. Kirkwood PA & Sears TA (1982). The effects of single afferent impulses on the probability of firing of external intercostal motoneurones in the cat. J Physiol 322, 315-336.
53. Knight BW (1972). Dynamics of encoding in a population of neurons. J General Physiol 59, 734-766.
54. Knox CK (1974). Cross-correlation functions for a neuronal model. Biophys J 14, 567-582.
55. Kuhn A, Aertsen A & Rotter S (2004). Neuronal integration of synaptic input in the fluctuation-driven regime. J Neurosci 24, 2345-2356.
56. Lapicque L (1907). Recherches quantitatifs sur l'excitation electrique des nerfs traitée comme une polarisation. J Physiol Paris 9, 620-635.
57. Lapicque L (1926). L'excitabilité En Founction Du Temps. Presses Universitaires de France, Paris, France.
58. Lee BB, Cleland BG & Creutzfeldt OD (1977). The retinal input to cells in area 17 of the cat's cortex. Exp Brain Res 30, 527-538.
59. Levick WR, Cleland BG & Dubin MW (1972). Lateral geniculate neurons of cat: retinal inputs and physiology. Invest Ophthalmol 11, 302-311.
60. Lindsey BG & Gerstein GL (1979). Interactions among an ensemble of chordotonal organ receptors and motor neurons of the crayfish claw. J Neurophysiol 42, 383-399.
61. Mainen ZF & Sejnowski TJ (1995). Reliability of spike timing in neocortical neurons. Science 268, 1503-1506.
62. Markram H, Lubke J, Frotscher M, Roth A & Sakmann B (1997a). Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500, 409-440.
63. Markram H, Lubke J, Frotscher M & Sakmann B (1997b). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215.
64. Mason A, Nicoll A & Stratford K (1991). Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J Neurosci 11, 72-84.
65. Mastronarde DN (1987). Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J Neurophysiol 57, 381-413.
66. Matsumura M, Chen D, Sawaguchi T, Kubota K & Fetz EE (1996). Synaptic interactions between primate precentral cortex neurons revealed by spike-triggered averaging of intracellular membrane potentials in vivo. J Neurosci 16, 7757-7767.
67. Miller LM, Escabi MA, Read HL & Schreiner CE (2001). Functional convergence of response properties in the auditory thalamocortical system. Neuron 32, 151-160.
68. Moore GP, Segundo JP, Perkel DH & Levitan H (1970). Statistical signs of synaptic interaction in neurons. Biophys J 10, 876-900.
69. Morris C & Lecar H (1981). Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35, 193-213.
70. Nagumo JS, Arimoto S & Yoshizawa S (1962). An active pulse transmission line simulating nerve axon. Proc IRE 50, 2061-2070.
71. Nowak LG, Sanchez-Vives MV & McCormick DA (1997). Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb Cortex 7, 487-501.
72. Palm G, Aertsen AM & Gerstein GL (1988). On the significance of correlations among neuronal spike trains. Biol Cybern 59, 1-11.
73. Perkel DH, Gerstein GL & Moore GP (1967). Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7, 419-440.
74. Poliakov AV, Powers RK & Binder MD (1997). Functional identification of the input-output transforms of motoneurones in the rat and cat. J Physiol 504, 401-424.
75. Pouille F & Scanziani M (2001). Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159-1163.
76. Reich DS, Victor JD, Knight BW, Ozaki T & Kaplan E (1997). Response variability and timing precision of neuronal spike trains in vivo. J Neurophysiol 77, 2836-2841.
77. Reid RC (2001). Divergence and reconvergence: multielectrode analysis of feedforward connections in the visual system. Prog Brain Res 130, 141-154.
78. Reid RC & Alonso JM (1995). Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281-284.
79. Reinagel P & Reid RC (2000). Temporal coding of visual information in the thalamus. J Neurosci 20, 5392-5400.
80. Reyes AD & Fetz EE (1993). Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. J Neurophysiol 69, 1661-1672.
81. Roy SA & Alloway KD (2001). Coincidence detection or temporal integration? What the neurons in somatosensory cortex are doing. J Neurosci 21, 2462-2473.
82. Singer W & Gray CM (1995). Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18, 555-586.
83. Sjostrom PJ, Turrigiano GG & Nelson SB (2001). Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149-1164.
84. So YT & Shapley R (1979). Spatial properties of X and Y cells in the lateral geniculate nucleus of the cat and conduction velocities of their inputs. Exp Brain Res 36, 533-550.
85. Song S, Miller KD & Abbott LF (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3, 919-926.
86. Stein RB (1967a). Some models of neuronal variability. Biophys J 7, 37-68.
87. Stein RB (1967b). The information capacity of nerve cells using a frequency code. Biophys J 7, 797-826.
88. Stratford KJ, Tarczy-Hornoch K, Martin KA, Bannister NJ & Jack JJ (1996). Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382, 258-261.
89. Stuart G & Sakmann B (1995). Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15, 1065-1076.
90. Surmeier DJ & Weinberg RJ (1985). The relationship between cross-correlation measures and underlying synaptic events. Brain Res 331, 180-184.
91. Swadlow HA (1995). Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation. J Neurophysiol 73, 1584-1599.
92. Swadlow HA, Beloozerova IN & Sirota MG (1998). Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J Neurophysiol 79, 567-582.
93. Swadlow HA, Gusev AG & Bezdudnaya T (2002). Activation of a cortical column by a thalamocortical impulse. J Neurosci 22, 7766-7773.
94. Tanaka K (1983). Cross-correlation analysis of geniculostriate neuronal relationships in cats. J Neurophysiol 49, 1303-1318.
95. Toyama K, Kimura M & Tanaka K (1981). Cross-correlation analysis of interneuronal connectivity in cat visual cortex. J Neurophysiol 46, 191-201.
96. Tuckwell HC (1988). Nonlinear and stochastic theory. In Introduction to Theoretical Neurobiology, Vol 2. Cambridge University Press, Cambridge.
97. Usrey WM, Reppas JB & Reid RC (1999). Specificity and strength of retinogeniculate connections. J Neurophysiol 82, 3527-3540.
98. Veredas FJ, Vico FJ & Alonso JM (2004). A computational tool to simulate correlated activity in neural circuits. J Neurosci Meth 136, 23-32.
99. Wehr M & Zador AM (2003). Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446.