Role of input correlations in shaping the variability and noise correlations of evoked activity in the neocortex

Journal of Neuroscience

Volumn 35, Issue 22, 2015, Pages 8611-8625

  Bujan, Alejandro F ^a   Aertsen, Ad ^a   Kumar, Arvind ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Attention; Evoked activity; Feedforward inputs; Network dynamics; Noise correlations; Trial by trial variability

Indexed keywords

AMPLITUDE MODULATION; ARTICLE; BRAIN DEPTH STIMULATION; CONDUCTANCE; DATA ANALYSIS; DYNAMICS; HUMAN; HUMAN CELL; MATHEMATICAL ANALYSIS; NEOCORTEX; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE POTENTIAL; NOISE; PRIORITY JOURNAL; SPIKE; STATISTICS; ACTION POTENTIAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; FEEDBACK SYSTEM; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; MODELS, NEUROLOGICAL; NEOCORTEX; NERVE NET; NEURONS; NOISE; STATISTICS AS TOPIC;

EID: 84930446843     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4536-14.2015     Document Type: Article

References (65)

1. Abbott LF, Dayan P (1999) The effect of correlated variability on the accuracy of a population code. Neural Comput 11:91–101.CrossRef Medline
2. Anderson EB, Mitchell JF, Reynolds JH (2011) Attentional modulation of firing rate varies with burstiness across putative pyramidal neurons in macaque visual area v4. J Neurosci 31:10983–10992.CrossRef Medline
3. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273:1868–1871.CrossRef Medline
4. Averbeck BB, Latham PE, Pouget A (2006) Neural correlations, population coding and computation. Nat Rev Neurosci 7:358–366.CrossRef Medline
5. Barlow H (1994) What is the computational goal of the neocortex? In: Large scale neuronal theories of the brain (Koch C, Davis JL, eds), pp 1–22. Cambridge, MA: Massachusetts Institute of Technology.
6. Barth AL, Poulet JF (2012) Experimental evidence for sparse firing in the neocortex. Trends Neurosci 35:345–355.CrossRef Medline
7. Bedenbaugh P, Gerstein GL (1997) Multiunit normalized cross correlation differs from the average single-unit normalized correlation. Neural Comput 9:1265–1275.CrossRef Medline
8. Boucsein C, Nawrot MP, Schnepel P, Aertsen A (2011) Beyond the cortical column: abundance and physiology of horizontal connections imply a strong role for inputs from the surround. Front Neurosci 5:32.CrossRef Medline
9. Braitenberg V, Schüz A (1998) Cortex: statistics and geometry of neuronal connectivity, Ed 2. Heidelberg: Springer.
10. Brette R (2009) Generation of correlated spike trains. Neural Comput 21: 188–215.CrossRef Medline
11. Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8:183–208.CrossRef Medline
12. Churchland MM, Yu BM, Cunningham JP, Sugrue LP, Cohen MR, Corrado GS, Newsome WT, Clark AM, Hosseini P, Scott BB, Bradley DC, Smith MA, Kohn A, Movshon JA, Armstrong KM, Moore T, Chang SW, Snyder LH, Lisberger SG, Priebe NJ, et al. (2010) Stimulus onset quenches neural variability: a widespread cortical phenomenon. Nat Neurosci 13:369–378.CrossRef Medline
13. Cohen MR, Maunsell JH (2009) Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12:1594–1600.CrossRef Medline
14. de la Rocha J, Doiron B, Shea-Brown E, Josić K, Reyes A (2007) Correlation between neural spike trains increases with firing rate. Nature 448:802–806.CrossRef Medline
15. Deco G, Hugues E (2012) Neural network mechanisms underlying stimulus driven variability reduction. PLoS Comput Biol 8:e1002395.CrossRef Medline
16. Doiron B, Lindner B, Longtin A, Maler L, Bastian J (2004) Oscillatory activity in electrosensory neurons increases with the spatial correlation of the stochastic input stimulus. Phys Rev Lett 93:048101.CrossRef Medline
17. Ecker AS, Berens P, Keliris GA, Bethge M, Logothetis NK, Tolias AS (2010) Decorrelated neuronal firing in cortical microcircuits. Science 327:584–587.CrossRef Medline
18. Eppler JM, Helias M, Muller E, Diesmann M, Gewaltig MO (2008) PyNEST: a convenient interface to the nest simulator. Front Neuroinform 2:12.CrossRef Medline
19. Gerstner W, Kistler WM (2002) Spiking neuron models: single neurons, populations, plasticity. Cambridge, MA: Cambridge UP.
20. Gewaltig MO, Diesmann M (2007) Nest (neural simulation tool). Scholarpedia 2:1430. CrossRef
21. Harris KD, Thiele A (2011) Cortical state and attention. Nat Rev Neurosci 12:509–523.CrossRef Medline
22. Helias M, Rotter S, Gewaltig MO, Diesmann M (2008) Structural plasticity controlled by calcium based correlation detection. Front Comput Neurosci 2:7.CrossRef Medline
23. Hennequin G, Vogels TP, Gerstner W (2014) Optimal control of transient dynamics in balanced networks supports generation of complex movements. Neuron 82:1394–1406.CrossRef Medline
24. Hong S, Ratté S, Prescott SA, De Schutter E (2012) Single neuron firing properties impact correlation-based population coding. J Neurosci 32: 1413–1428.CrossRef Medline
25. Hunter JD (2007) Matplotlib: A 2d graphics environment. Comput Sci Eng 9:90–95. CrossRef
26. Kriener B, Helias M, Aertsen A, Rotter S (2009) Correlations in spiking neuronal networks with distance dependent connections. J Comput Neurosci 27:177–200.CrossRef Medline
27. Kuhn A, Aertsen A, Rotter S (2003) Higher-order statistics of input ensembles and the response of simple model neurons. Neural Comput 15:67–101.CrossRef Medline
28. Kumar A, Rotter S, Aertsen A (2008) Conditions for propagating synchronous spiking and asynchronous firing rates in a cortical network model. J Neurosci 28:5268–5280.CrossRef Medline
29. Kumar A, Rotter S, Aertsen A (2010) Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding. Nat Rev Neurosci 11:615–627.CrossRef Medline
30. Lindner B, Doiron B, Longtin A (2005) Theory of oscillatory firing induced by spatially correlated noise and delayed inhibitory feedback. Phys Rev E Stat Nonlin Soft Matter Phys 72:061919.CrossRef Medline
31. Lindsay G, Bujan A, Aertsen A, Kumar A (2012) Within versus between correlations and their relation to the network structure. In Neuroscience Meeting Planner. New Orleans: Society for Neuroscience Program No. 712.04/FFF64.
32. Litwin-Kumar A, Doiron B (2012) Slow dynamics and high variability in balanced cortical networks with clustered connections. Nat Neurosci 15: 1498–1505.CrossRef Medline
33. Maimon G, Assad JA (2009) Beyond poisson: increased spike-time regularity across primate parietal cortex. Neuron 62:426–440.CrossRef Medline
34. Mehring C, Hehl U, Kubo M, Diesmann M, Aertsen A (2003) Activity dynamics and propagation of synchronous spiking in locally connected random networks. Biol Cybern 88:395–408.CrossRef Medline
35. Mitchell JF, Sundberg K, Reynolds JH (2007) Differential attentiondependent response modulation across cell classes in visual area v4. Neuron 55:1–14.CrossRef Medline
36. Mitchell JF, Sundberg KA, Reynolds JH (2009) Spatial attention decorrelates intrinsic activity fluctuations in macaque area v4. Neuron 63:879–888.CrossRef Medline
37. Moreno-Bote R, Parga N (2006) Auto and crosscorrelograms for the spike response of leaky integrate-and-fire neurons with slow synapses. Phys Rev Lett 96:028101.CrossRef Medline
38. Moreno-Bote R, Renart A, Parga N (2008) Theory of input spike autoand cross-correlations and their effect on the response of spiking neurons. Neural Comput 20:1651–1705.CrossRef Medline
39. Nawrot MP, Boucsein C, Rodriguez Molina V, Riehle A, Aertsen A, Rotter S (2008) Measurement of variability dynamics in cortical spike trains. J Neurosci Methods 169:374–390.CrossRef Medline
40. Oram MW (2011) Visual stimulation decorrelates neuronal activity. J Neurophysiol 105:942–957.CrossRef Medline
41. Rajan K, Abbott LF, Sompolinsky H (2010) Stimulus-dependent suppression of chaos in recurrent neural networks. Phys Rev E Stat Nonlin Soft Matter Phys 82:011903.CrossRef Medline
42. 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.CrossRef Medline
43. Ricciardi LM (1977) Diffusion processes and related topics in biology. New York: Springer.
44. Rosenbaum R, Josić K (2011) Mechanisms that modulate the transfer of spiking correlations. Neural Comput 23:1261–1305.CrossRef Medline
45. Rosenbaum R, Trousdale J, Josić K (2010) Pooling and correlated neural activity. Front Comput Neurosci 4:9.CrossRef Medline
46. Rosenbaum R, Trousdale J, Josić K (2011) The effects of pooling on spike train correlations. Front Neurosci 5:58.CrossRef Medline
47. Ruff DA, Cohen MR (2014) Attention can either increase or decrease spike count correlations in visual cortex. Nat Neurosci 17:1591–1597.CrossRef Medline
48. Salinas E, Sejnowski TJ (2000) Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J Neurosci 20: 6193–6209. Medline
49. Salinas E, Sejnowski TJ (2002) Integrate-and-fire neurons driven by correlated stochastic input. Neural Comput 14:2111–2155.CrossRef Medline
50. Schnepel P, Kumar A, Zohar M, Aertsen A, Boucsein C (2014) Physiology and impact of horizontal connections in rat neocortex. Cereb Cortex. Advance online publication. Retrieved Nov. 19, 2014. doi: 10.1093/cercor/bhu265.CrossRef Medline
51. Schultze-Kraft M, Diesmann M, Grün S, Helias M (2013) Noise suppression and surplus synchrony by coincidence detection. PLoS Comput Biol 9:e1002904.CrossRef Medline
52. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870–3896. Medline
53. Smith MA, Kohn A (2008) Spatial and temporal scales of neuronal correlation in primary visual cortex. J Neurosci 28:12591–12603.CrossRef Medline
54. 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
55. Staude B, Rotter S, Grün S (2008) Can spike coordination be differentiated from rate covariation? Neural Comput 20:1973–1999.CrossRef Medline
56. Staude B, Rotter S, Grün S (2010) Cubic: cumulant based inference of higher-order correlations in massively parallel spike trains. J Comput Neurosci 29:327–350.CrossRef Medline
57. Tetzlaff T, Helias M, Einevoll GT, Diesmann M (2012) Decorrelation of neural-network activity by inhibitory feedback. PLoS Comput Biol 8:e1002596.CrossRef Medline
58. Vogels TP, Abbott LF (2009) Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat Neurosci 12: 483–491.CrossRef Medline
59. Voges N, Perrinet L (2012) Complex dynamics in recurrent cortical networks based on spatially realistic connectivities. Front Comput Neurosci 6:41.CrossRef Medline
60. Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442.CrossRef Medline
61. White B, Abbott LF, Fiser J (2012) Suppression of cortical neural variability is stimulus-and state-dependent. J Neurophysiol 108:2383–2392.CrossRef Medline
62. Yannaros N (1988) On Cox processes and gamma renewal processes. J Appl Physiol 423–427.
63. Yger P, El Boustani S, Destexhe A, Frégnac Y (2011) Topologically invariant macroscopic statistics in balanced networks of conductance-based integrate-and-fire neurons. J Comput Neurosci 31:229–245.CrossRef Medline
64. Yim MY, Aertsen A, Kumar A (2011) Significance of input correlations in striatal function. PLoS Comput Biol 7:e1002254.CrossRef Medline
65. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140–143.CrossRef Medline