Decoding temporal information: A model based on short-term synaptic plasticity

Journal of Neuroscience

Volumn 20, Issue 3, 2000, Pages 1129-1141

  Buonomano, Dean V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Interval; Paired pulse depression; Paired pulse facilitation; Short term plasticity; Temporal processing; Timing

Indexed keywords

ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PRIORITY JOURNAL;

EID: 0034143330     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-03-01129.2000     Document Type: Article

References (82)

1. Abbott LF, Varela JA, Kamal S, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220-224.
2. Adler TB, Rose GJ (1998) Long-term temporal integration in the anuran auditory system. Nat Neurosci 1:519-523.
3. Ahissar E, Haidarliu S, Zacksenhouse M (1997) Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. Proc Natl Acad Sci USA 94:11633-11638.
4. Beaulieu C, Kisvarday Z, Somogyi P, Cynader M, Cowey A (1992) Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb Cortex 2:295-309.
5. Braitenherg V (1967) Is the cerebellar cortex a biological clock in the millisecond range? Prog Brain Res 25:334-336.
6. Brown TH, Fricke RA, Ferkel DH (1981) Passive electrical constants in three classes of hippocampal neurons. J Neurophysiol 46:812-827.
7. Buonomano DV, Mauk MD (1994) Neural network model of the cerebellum: temporal discrimination and the timing of motor responses. Neural Comput 6:38-55.
8. Buonomano DV, Merzenich MM (1995) Temporal information transformed into a spatial code by a neural network with realistic properties. Science 267:1028-30.
9. Buonomano DV, Merzenich MM (1996) Associative synaptic plasticity in hippocampal CA1 neurons is not sensitive to unpaired presynaptic activity. J Neurophysiol 76:631-636.
10. Buonomano DV, Merzenich MM (1998) Net interaction between different forms of short-term synaptic plasticity and slow-IPSPs in the hippocampus and auditory cortex. J Neurophysiol 80:1765-1774.
11. Buonomano DV, Merzenich MM (1999) A neural network model of temporal code generation of position invariant pattern recognition. Neural Comput 11:103-116.
12. Buonomano DV, Hickmott PW, Merzenich MM (1997) Temporal to spatial transformations and context-sensitive plasticity in hippocampal slices. Proc Natl Acad Sci USA 94:10403-10408.
13. Carr CE (1993) Processing of temporal information in the brain. Annu Rev Neurosci 16:223-243.
14. Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264:847-850.
15. Creager R. Dunwiddie T, Lynch G (1980) Paired-pulse and frequency facilitation in the CA1 region of the in vitro hippocampus. J Physiol (Lond) 299:409-424.
16. Creelman CD (1962) Human discrimination of auditory duration. J Acoust Soc Am 34:582-593.
17. Creutzfeldt O, Ojemann G, Lettich E (1989) Neuronal activity in the human lateral temporal lobe. I. Responses to speech. Exp Brain Res 77:451-475.
18. Davies CH, Davies SN, Collingridge GL (1990) Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol (Lond) 424:513-531.
19. Deisz RA, Prince DA (1989) Frequency-dependent depression of inhibition in guinea-pig neocortex in vitro by GABAB receptor feed-back on GABA release. J Physiol (Lond) 412:513-541.
20. Destexhe A, Mainen ZF, Sejnowski TJ (1993) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comput 6:14-18.
21. Doupe AJ, Konishi M (1991) Song-selective auditory circuits in the vocal control system of the zebra finch. Proc Natl Acad Sci USA 88:11339-11343.
22. Fiala JC, Grossberg S, Bullock D (1996) Metabotropic glutamate receptor activation in cerebellar Purkinje Cells as substrate for adaptive timing of the classically conditioned eye-blink response. J Neurosci 16:3760-3734.
23. Fisher SA, Fischer SA, Carew TJ (1997) Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci 20:170-177.
24. Fukuda A, Mody I, Prince DA (1993) Differential ontogenesis of presynaptic and postsynaptic GABAB inhibition in rat somatosensory cortex. J Neurophysiol 70:448-452.
25. Galarreta M, Hestrin S (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1:587-594.
26. Gibbon J, Malapani C, Dale CL, Gallistel CR (1997) Toward a neurobiology of temporal cognition: advances and challenges. Curr Opin Neurobiol 7:170-184.
27. Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19: 679-686.
28. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385-397.
29. Golomb D, Wang XJ, Rinzel J (1994) Synchronization properties of spindle oscillations in a thalamic reticular nucleus model. J Neurophysiol 72:1109-1126.
30. Hablitz JJ, Thalmann RH (1987) Conductance changes underlie a late synaptic hyperpolarization in hippocampal CA3 neurons. J Neurophysiol 58:160-179.
31. Harrington DL, Haaland KY, Knight RT (1998a) Cortical networks underlying mechanisms of time perception. J Neurosci 18:1085-1095.
32. Harrington DL, Haaland KY, Hermanowicz N (1998b) Temporal processing in the basal ganglia. Neuropsychology 12:3-12.
33. He J, Hashikawa T, Ojima H, Kinouchi Y (1997) Temporal integration and duration tuning in the dorsal zone of the cat auditory cortex. J Neurosci 17:2615-2626.
34. Hines ML, Moore JW (1997) Computer simulations with NEURON. http://neuron.duke.edu/.
35. Ivry R (1996) The representation of temporal information in perception and motor control. Curr Opin Neurobiol 6:851-857.
36. Ivry R, Keele S (1989) Timing function of the cerebellum. J Cognit Neurosci 1:136-152.
37. Jeffress LA (1948) A place theory of sound localization J Comp Physiol Psychol 41:35-39.
38. Lacaille J-C, Mueller K, Schwartzkroin PA (1987) Local circuit interaction between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993.
39. Lambert NA, Wilson WA (1993) Discrimination of post- and presynaptic GABAB receptor-mediated responses by tetrahydroaminnoacridine in area CA3 of the rat hippocampus. J Neurophysiol 69:630-635.
40. Lewicki MS, Arthur BJ (1996) Hierarchical organization of auditory temporal context sensitivity. J Neurosci 16:6987-6998.
41. Manabe T, Wyllie DJA, Perkel DJ, Nicoll RA (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSP variance in the CA1 region of the hippocampus. J Neurophysiol 70:1451-1459.
42. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol (Lond) 500:409-440.
43. Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95:5323-5328.
44. Margoliash D (1983) Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci 3:1039-1057.
45. 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.
46. Mauk MD, Donegan NH (1997) A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn Mem 4:130-158.
47. McClurkin JW, Optican LM, Richmond BJ, Gawne TJ (1991) Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. Science 253:675-677.
48. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
49. Mechler R, Victor JD, Purpura KP, Shapley R (1998) Robust temporal coding of contrast by V1 neurons for transient but not for steady-state stimuli. J Neurosci 18:6583-6598.
50. Miall C (1989) The storage of time intervals using oscillating neurons. Neural Comput 1:359-371.
51. Middlebrooks JC, Clock AE, Xu L, Green DM (1994) A panoramic code for sound location by cortical neurons. Science 264:842-844.
52. Nagarajan SS, Blake DT, Wright BA, Byl N, Merzenich MM (1998) Practice-related improvements in somatosensory interval discrimination are temporally specific but generalize across skin location, hemisphere and modality. J Neurosci 18:1559-1570.
53. Nathan T, Lambert JDC (1991) Depression of the fast IPSP underlies paired-pulse facilitation in area CA1 of the rat hippocampus. J Neurophysiol 66:1704-1715.
54. Newberry NR, Nicoll NA (1984) A bicuculline-resistant inhibitory postsynaptic potential in rat hippocampal pyramidal cells in vitro. J Physiol (Lond) 348:239-254.
55. Olpe HR, Steinmann MW, Greiner K, Pozza MF (1994) Contribution of presynaptic GABA-B receptors to paired-pulse depression of GABA-responses in the hippocampus. Naunyn Schmiedebergs Arch Pharmacol 349:473-477.
56. Olsen JF, Suga N (1991) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of the target range information. J Neurophysiol 65:1275-1289.
57. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13:1708-1718.
58. Prut Y, Vaadia E, Berman H, Haalman I, Solvin H, Abeles H (1998) Spatiotemporal structure of cortical activity: properties and behavioral relevance. J Neurophysiol 2857-2874.
59. Ramoa AS, Sur M (1996) Short-term synaptic plasticity in the visual cortex during development. Cereb Cortex 6:640-646.
60. Rauschecker JP, Tian B, Hauser M (1995) Processing complex sounds in the macaque nonprimary auditory cortex. Science 268:111-114.
61. Reyes A, Sakmann B (1998) Layer specific and developmentally regulated short-term modification of unitary EPSPs in neocortical pyramidal neurons. Soc Neurosci Abstr 24:318.
62. Reyes A, Lujan R, Burnashev N, Somogyi P, Sakmann B (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1:279-285.
63. Richmond BJ, Optican LM, Spitzer H (1990) Temporal encoding of two-dimensional patterns by single units in primate visual cortex. I Stimulus-response relations. J Neurophysiol 64: 351-368.
64. Riquimaroux R (1994) Neuronal auditory scene analysis? Trans Tech Comm Psychol Physiol Acoust Soc Jpn (H) 28:1-8.
65. Rumelhart DE, McClelland JL (1986) Parallel distributed processing. Cambridge: MIT.
66. Saitoh I, Suga N (1995) Long delay lines for ranging are created by inhibition in the inferior colliculus of the mustached bat. J Neurophysiol 74:1-11.
67. Salin PS, Scanziani M, Malenka RC, Nicoll RA (1996) Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93:13304-13309.
68. Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303-304.
69. Stratford KJ, Tarczy-Hornoch K, Martin KAC, Bannister NJ, Jack JJB (1996) Excitatory synaptic inputs to spiky stellate cells in cat visual cortex. Nature 382:258-261.
70. Sullivan WE (1982) Possible neural mechanisms of target distance coding in the auditory system of the echolocating bat Myotis lucifugus. J Neurophysiol 48:1033-1047.
71. Tallal P (1994) In the perception of speech time is of the essence. In: Temporal coding in the brain (Buzsaki G, Llinas R, Singer W, Berthoz A, Christen Y, eds), pp 291-299. Berlin: Springer.
72. Tank DW, Hopfield JJ (1987) Neural computation by concentrating information in time. Proc Natl Acad Sci USA 84:1896-1900.
73. Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17:120-126.
74. Thomson AM, West DC (1993) Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex. Neuroscience 54:329-346.
75. Thomson AM, Girdlestone D, West DC (1988) Voltage-dependent currents prolong single-axon postsynaptic potentials in layer III pyramidal neurons in rat neocortical slices. J Neurophysiol 60:1896-1907.
76. Thomson AM, Deuchars J, West DC (1993) Single axons excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation. Neuroscience 54:347-360.
77. Traub RD, Miles R, Buzsáki G (1992) Computer simulation of carbachol-driven rhythmic population oscillations in trie CA3 region of the in vitro rat hippocampus. J Physiol (Lond) 451:653-672.
78. Treisman M (1963) Temporal discrimination and the indifference interval: implications for a model of the "internal clock". Psychol Monogr 77:1-31.
79. Wang X, Merzenich MM, Beitel R, Schreiner CE (1995) Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74:2685-2706.
80. Wright BA, Buonomano DV, Mahncke HW, Merzenich MM (1997) Learning and generalization of auditory temporal-interval discrimination in humans. J Neurosci 17: 3956-3963.
81. Zalutsky RA, Nicoll RA (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248:1619-1624.
82. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.