Short-term plasticity explains irregular persistent activity in working memory tasks

Journal of Neuroscience

Volumn 33, Issue 1, 2013, Pages 133-149

  Hansel, David ^a   Mato, German ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; N METHYL DEXTRO ASPARTIC ACID;

ARTICLE; COMPUTER MODEL; COMPUTER SIMULATION; DEPTH PERCEPTION; EYE MOVEMENT CONTROL; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; SENSORY STIMULATION; SPIKE WAVE; SYNAPTIC TRANSMISSION; VISUAL FIELD; WORKING MEMORY;

ACTION POTENTIALS; HUMANS; MEMORY, SHORT-TERM; MODELS, NEUROLOGICAL; NERVE NET; NEURONAL PLASTICITY; NEURONS; PREFRONTAL CORTEX; SYNAPSES;

EID: 84871821796     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3455-12.2013     Document Type: Article

References (84)

1. Amit DJ, Brunel N (1997) Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. Cereb Cortex 7:237-252. CrossReRef Medline
2. Amit DJ (1995) Modeling brain functions: the world of attractor neural networks. Cambridge, UK: Cambridge UP.
3. Arguello PA, Gogos JA (2012) Genetic and cognitive windows into circuit mechanisms of psychiatric disease. Trends Neurosci 35:3-13. CrossReRef Medline
4. Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:1399-1407. CrossReRef Medline
5. Baddeley AD (1986) Working memory. Oxford, UK: Oxford UP.
6. Bair W, Koch C, Newsome W, Britten K (1994) Power spectrum analysis of bursting cells in area MT in the behaving monkey. J Neurosci 14:2870-2892. Medline
7. Barbieri F, Brunel N (2008) Can attractor network models account for the statistics of firing during persistent activity in prefrontal cortex? Front Neurosci 2:114-122. CrossReRef Medline
8. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687-2698. Medline
9. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci U S A 99:13222-13227. CrossReRef Medline
10. Ben-Yishai R, Lev Bar-Or RL, Sompolinsky H (1995) Theory of orientation tuning in visual cortex. Proc Natl Acad SciU S A 92:3844-3848. CrossReRef Medline
11. Brody CD, Hernández A, Zainos A, Romo R (2003) Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb Cortex 13:1196-1207. CrossReRef Medline
12. Brunel N (2000) Persistent activity and the single-cell frequency-current curve in a cortical network model. Network 11:261-280. CrossReRef Medline
13. Burns BD, Webb AC (1976) The spontaneous activity of neurones in the cat's cerebral cortex. Proc R Soc Lond B Biol Sci 194:211-223. CrossReRef Medline
14. Camperi M, Wang XJ (1998) A model of visuospatial working memory in prefrontal cortex: recurrent network and cellular bistability. J Comput Neurosci 5:383-405. CrossReRef Medline
15. Compte A, Brunel N, Goldman-Rakic PS, Wang XJ (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10:910-923. CrossReRef Medline
16. Compte A, Constantinidis C, Tegner J, Raghavachari S, Chafee MV, Goldman-Rakic PS, Wang, XJ (2003) Temporally irregular mnemonic persistent activity in prefrontal neurons of monkeys during a delayed response task. J Neurophysiol 90:3441-3454. CrossReRef Medline
17. Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48:1302-1320. Medline
18. Constantinidis C, Franowicz MN, Goldman-Rakic PS (2001) The sensory nature of mnemonic representation in the primate prefrontal cortex. Nat Neurosci 4:311-316. CrossReRef Medline
19. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. Cambridge, MA: MIT.
20. Destexhe A, Rudolph M, Pare ́ D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751. CrossReRef Medline
21. Durstewitz D, Gabriel T (2007) Dynamical basis of irregular spiking in NMDA-driven prefrontal cortex neurons. Cereb Cortex 17:894-908. Medline
22. Fe ́nelon K, Mukai J, Xu B, Hsu PK, Drew LJ, Karayiorgou M, Fischbach GD, Macdermott AB, Gogos JA (2011) Deciency of Dgcr8, a gene disrupted by the 22q11.2 microdeletion, results in altered short-term plasticity in the prefrontal cortex. Proc Natl Acad Sci U S A 108:4447-4452. CrossReRef Medline
23. Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331-349. Medline
24. Funahashi S, Bruce CJ, Goldman-Rakic PS (1990) Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. J Neurophysiol 63:814-831. Medline
25. Funahashi S, Bruce CJ, Goldman-Rakic PS (1991) Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 65:1464-1483. Medline
26. Fuster JM (2008) The prefrontal cortex. Fourth edition. London, UK: Elsevier.
27. Fuster JM, Alexander GE (1971) Neuron activity related to short-term memory. Science 173:652-654. CrossReRef Medline
28. Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Handbook of physiology. The nervous system. Higher functions of the brain, pp 373-417. Bethesda, MD: American Physiological Society.
29. Goldman-Rakic PS (1988) Topography of cognition. Parallel distributed networks in primate association cortex. Annu Rev Neurosci 11:137-156. CrossReRef Medline
30. Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14: 477-485. CrossReRef Medline
31. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545. CrossReRef Medline
32. Hansel D, Mato G (2008) Balanced excitation and inhibition and shortterm plasticity: a new paradigm for working memory. Abstract Soc Neurosci. Washington, 2008.
33. Hansel D, Sompolinsky H (1996) Chaos and synchrony in a model of a hypercolumn in visual cortex. J Comput Neurosci 3:7-34. CrossReRef Medline
34. Hansel D, Sompolinsky H (1998) Modeling feature selectivity in local cortical circuits. In: Methods in neuronal modeling. From synapses to networks. Second edition (Koch C, Segev I, eds). Cambridge, MA: MIT.
35. Hansel D, van Vreeswijk C (2012) The mechanism of orientation selectivity in primary visual cortex without a functional map. J Neurosci 32:4049-4064. CrossReRef Medline
36. Hansel D, Mato G, Meunier C, Neltner L (1998) On numerical simulations of integrate-and-fire neural networks. Neural Comput 10:467-483. CrossReRef Medline
37. Hebb DO (1949) The organization of behavior. New York: Wiley.
38. Hempel CM, Hartman KH, Wang XJ, Turrigiano GG, Nelson SB (2000) Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. J Neurophysiol 83:3031-3041. Medline
39. Hertz J (2010) CrossRe-correlations in high-conductance states of a model cortical network. Neural Comput 22:427-447. Medline
40. Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75:1806-1814. Medline
41. Hopfield JJ (1984) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci U S A 81:3088-3092. Medline
42. Itskov V, Hansel D, Tsodyks M (2011) Short-term facilitation may stabilize parametric working memory trace. Front Comput Neurosci 5:1-19. Medline
43. Jahr CE, Stevens CF (1990) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10: 3178:3182.
44. Lerchner A, Ahmadi M, Hertz J (2004) High-conductance states in a meanfield cortical network model. Neurocomputing 58:935-940. CrossReRef
45. Lerchner A, Ursta C, Hertz J, Ahmadi M, Ruffiot P, Enemark S (2006) Response variability in balanced cortical networks. Neural Comput 18:634-659. CrossReRef Medline
46. Lundqvist M, Compte A, Lansner A (2010) Bistable, irregular firing and population oscillations in a modular attractor memory network. PLos Comput Biol 6:e1000803. CrossReRef Medline
47. Maimon G, Assad JA (2009) Beyond Poisson: increased spike-time regularity across primate parietal cortex. Neuron 62:426-440. CrossReRef Medline
48. Mardia KV (1972) Statistics of directional data. London, UK: Academic.
49. Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neorcortical pyramidal neurons. Proc Natl Acad Sci U S A 95: 5323-5328. CrossReRef Medline
50. Miyashita Y, Chang HS (1988) Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331:68-70. CrossReRef Medline
51. Mongillo G, Barak O, Tsodyks M (2008) Synaptic theory of working memory. Science 319:1543-1546. CrossReRef Medline
52. Mongillo G, Hansel D, van Vreeswijk C (2012) Bistability and spatiotemporal irregularity in neuronal networks with nonlinear synaptic transmission. Phys Rev Lett 108:158101. CrossReRef Medline
53. Ploner CJ, Gaymard B, Rivaud S, Agid Y, Pierrot-Deseilligny C (1998) Temporal limits of spatial working memory in humans. Eur J Neurosci 10: 794-797. CrossReRef Medline
54. Press W, Vetterling W, Teukolsky S, Flannery B (1992) Numerical recipes in FORTRAN 77: the art of scientific computing. Cambridge, UK: Cambridge UP.
55. Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization. J Neurophysiol 81:1903-1916. Medline
56. Renart A, Song P, Wang XJ (2003) Robust spatial working memory through homeostatic synaptic scaling in heterogeneous cortical networks. Neuron 38:473-485. CrossReRef Medline
57. Renart A, Moreno-Bote R, Wang XJ, Parga N (2007) Mean-driven and fluctuation-driven persistent activity in recurrent networks. Neural Comput 19:1-46. CrossReRef Medline
58. Renart A, de la Rocha J, Bartho P, Hollender L, Parga N, Reyes A, Harris KD (2010) The asynchronous state in cortical circuits. Science 327:587-590. CrossReRef Medline
59. Romo R, Brody CD, Hernández A, Lemus L (1999) Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399: 470-473. CrossReRef Medline
60. Roudi Y, Latham PE (2007) A balanced memory network. PLoS Comput Biol 3:e141. CrossReRef Medline
61. Seung HS, Lee DD, Reis BY, Tank DW (2000) Stability of the memory of eye position in a recurrent network of conductance-based model neurons. Neuron 26:259-271. CrossReRef Medline
62. Shafi M, Zhou Y, Quintana J, Chow C, Fuster J, Bodner M (2007) Variability in neuronal activity in primate cortex during working memory tasks. Neuroscience 146:1082-1108. CrossReRef Medline
63. Shinomoto S, Kim H, Shimokawa T, Matsuno N, Funahashi S, Shima K, Fujita I, Tamura H, Doi T, Kawano K, Inaba N, Fukushima K, Kurkin S, Kurata K, Taira M, Tsutsui K, Komatsu H, Ogawa T, Koida K, Tanji J, et al. (2009) Relating neuronal firing patterns to functional differentiation of cerebral cortex. PLoS Comput Biol 5:e1000433. CrossReRef Medline
64. Shinomoto S, Sakai Y, Funahashi S (1999) The Ornstein-Uhlenbeck process does not reproduce spiking statistics of neurons in prefrontal cortex. Neural Comput 11:935-951. CrossReRef Medline
65. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293. CrossReRef Medline
66. Softky WR, Koch C (1992) Cortical cells should fire regularly, but do not. Neural Comput 4:643-646. CrossReRef
67. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334-350. Medline
68. Somers DC, Nelson SB, Sur M (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci 15:5448-5465. Medline
69. Takeda K, Funahashi S (2002) Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks. J Neurophysiol 87:567-588. Medline
70. Takeda K, Funahashi S (2007) Relationship between prefrontal task-related activity and information flow during spatial working memory performance. Cortex 43:38-52. CrossReRef Medline
71. Thomson AM (1997) Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiology 502:131-147. CrossReRef Medline
72. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94:719-723. CrossReRef Medline
73. Tsodyks M, Sejnowski T (1995) Rapid switching in balanced cortical network models. Network 6:1-14. CrossReRef
74. Tsodyks M, Sejnowski T (1997) Associative memory and hippocampal place cells. Adv Neural Inf Process Syst 6:81-86.
75. van Vreeswijk C, Sompolinsky H (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724-1726. CrossReRef Medline
76. van Vreeswijk C, Sompolinsky H (1998) Chaotic balanced state in a model of cortical circuits. Neural Comput 10:1321-1371. CrossReRef Medline
77. van Vreeswijk C, Sompolinsky H (2004) Irregular activity in large networks of neurons. In: Methods and models in neurophysics, lecture notes of the XXX Les Houches Summer School (Chow C, Gutkin B, Hansel D, Meunier C, Dalibard J, eds). London, UK: Elsevier Science and Technology.
78. Vogels TP, Abbott LF (2009) Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat Neurosci 12: 483-491. CrossReRef Medline
79. Vogels TP, Rajan K, Abbott LF (2005) Neural network dynamics. Annual Rev Neurosci 28:357-376. CrossReRef
80. Wang H, Stradtam GG 3rd, Wang XJ, Gao WJ (2008) A specialized NMDA receptor function in layer 5 recurrent microcircuitry of the adult rat prefrontal cortex. Proc Natl Acad Sci U S A 105:16791-16796. CrossReRef Medline
81. Wang XJ (2001) Synaptic reverberations underlying mnemonic persistent activity. Trends Neurosci 24:455-463. Medline
82. Wang Y, Markram H, Goodman PH, Berger TK, Ma J, Goldman-Rakic PS (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci 9:534-542. CrossReRef Medline
83. White JM, Sparks DL, Stanford TR (1994) Saccades to remembered target locations: an analysis of systematic and variable errors. Vision Res 34:79-92. CrossReRef Medline
84. Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112-2126. Medline