Cortical state determines global variability and correlations in visual cortex

Journal of Neuroscience

Volumn 35, Issue 1, 2015, Pages 170-178

  Schölvinck, Marieke L ^a   Saleem, Aman B ^a   Benucci, Andrea ^a,c   Harris, Kenneth D ^a,b   Carandini, Matteo ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Brain states; Cerebral cortex; Neural populations; Thalamus; Vision

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; FEMALE; LATERAL GENICULATE BODY; NERVE POTENTIAL; NONHUMAN; RESPONSE VARIABILITY; SPIKE WAVE; STIMULUS; STIMULUS RESPONSE; STRIATE CORTEX; VISUAL CORTEX; ANIMAL; CAT; NERVE CELL NETWORK; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; RANDOMIZATION; VISUAL SYSTEM;

ANIMALS; CATS; FEMALE; NERVE NET; PHOTIC STIMULATION; RANDOM ALLOCATION; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84920544032     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4994-13.2015     Document Type: Article

References (62)

1. 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.
2. 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.
3. Bair W, Zohary E, Newsome WT (2001) Correlated firingin macaque visual area MT: time scales and relationship to behavior. J Neurosci 21:1676-1697.
4. Benucci A, Ringach DL, Carandini M (2009) Coding of stimulus sequences by population responses in visual cortex. Nat Neurosci 12:1317–1324.
5. Bonin V (2005) Contrast gain control, noise, and spike threshold in the early visual system. PhD Thesis. Zurich: Swiss Federal Institute of Technology.
6. Bonin V, Mante V, Carandini M (2003) Predicting signal and noise in LGN and V1. Program No. 229.5. In: Online Abstract Viewer. Washington, DC: Society for Neuroscience.
7. Bonin V, Mante V, Carandini M (2005) The suppressive field of neurons in lateral geniculate nucleus. J Neurosci 25:10844–10856.
8. Bradley A, Skottun BC, Ohzawa I, Sclar G, Freeman RD (1987) Visual orientation and spatial frequency discrimination: a comparison of single neurons and behavior. J Neurophysiol 57:755–772.
9. 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.
10. Buracas GT, Zador AM, DeWeese MR, Albright TD (1998) Efficient discrimination of temporal patternsby motion-sensitive neurons in primate visual cortex. Neuron 20:959–969.
11. Carandini M (2004) Amplification of trial-to-trial response variability by neurons in visual cortex. PLoS Biol 2:E264.
12. Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20:470–484.
13. Ch’ng YH, Reid RC (2010) Cellular imaging of visual cortex reveals the spatial and functional organization of spontaneous activity. Front Integr Neurosci 4:pii20.
14. Clement EA, Richard A, Thwaites M, Ailon J, Peters S, Dickson CT (2008) Cyclic and sleep-like spontaneous alternations of brain state under ure-thane anaesthesia. PLoS One 3:e2004.
15. Cohen MR, Kohn A (2011) Measuring and interpreting neuronal correlations. Nat Neurosci 14:811–819.
16. Cohen MR, Maunsell JH (2009) Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12:1594–1600.
17. Curto C, Sakata S, Marguet S, Itskov V, Harris KD (2009) A simple model of cortical dynamics explains variability and state dependence of sensory responses in urethane-anesthetized auditory cortex. J Neurosci 29: 10600–10612.
18. Dean AF (1981) The variability of discharge of simple cells in the cat striate cortex. Exp Brain Res 44:437–440.
19. Deweese MR, Zador AM (2004) Shared and private variability in the auditory cortex. J Neurophysiol 92:1840–1855.
20. Dinstein I, Heeger DJ, Lorenzi L, Minshew NJ, Malach R, Behrmann M (2012) Unreliable evoked responses in autism. Neuron 75:981–991.
21. Durand S, Freeman TC, Carandini M (2007) Temporal properties of surround suppressionincat primary visual cortex. Vis Neurosci 24:679–690.
22. Ecker AS, Berens P, Keliris GA, Bethge M, Logothetis NK, Tolias AS (2010) Decorrelated neuronal firing in cortical microcircuits. Science 327:584-587.
23. Ecker AS, Berens P, Cotton RJ, Subramaniyan M, Denfield GH, Cadwell CR, Smirnakis SM, Bethge M, Tolias AS (2014) State dependence of noise correlations in macaque primary visual cortex. Neuron 82:235–248.
24. Geisler WS, Albrecht DG (1997) Visual cortex neuronsin monkeys and cats: detection, discrimination, and identification. Vis Neurosci 14:897–919.
25. Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12:1444–1449.
26. Goris RL, Movshon JA, Simoncelli EP (2014) Partitioning neuronal variability. Nat Neurosci 17:858–865.
27. Greenberg DS, Houweling AR, Kerr JN (2008) Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat Neurosci 11:749–751.
28. Harris KD, Thiele A (2011) Cortical state and attention. Nat Rev Neurosci 12:509–523.
29. Harris KD, Csicsvari J, Hirase H, Dragoi G, Buzsáki G (2003) Organization of cell assemblies in the hippocampus. Nature 424:552–556.
30. Heggelund P, Albus K (1978) Response variability and orientation discrimination of single cells in striate cortex of cat. Exp Brain Res 32:197–211.
31. Kara P, Reinagel P, Reid RC (2000) Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27:635-646.
32. Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A (2003) Spontaneously emerging cortical representations of visual attributes. Nature 425: 954–956.
33. Kisley MA, Gerstein GL (1999) Trial-to-trial variability and state-dependent modulation of auditory-evoked responses in cortex. J Neuro-sci 19:10451–10460.
34. Ko H, Hofer SB, Pichler B, Buchanan KA, Sjöstrom PJ, Mrsic-Flogel TD (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473:87–91.
35. Kohn A, Smith MA (2005) Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J Neurosci 25:3661–3673.
36. Kohn A, Zandvakili A, Smith MA (2009) Correlations and brain states: from electrophysiology to functional imaging. Curr Opin Neurobiol 19:434-438.
37. Levine MW, Troy JB (1986) The variability of the maintained discharge of cat dorsal lateral geniculate cells. J Physiol 375:339–359.
38. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503–1506.
39. Mante V, Bonin V, Carandini M (2008) Functional mechanisms shaping lateral geniculate responses to artificial and natural stimuli. Neuron 58: 625–638.
40. Marguet SL, Harris KD (2011) State-dependent representation of amplitude-modulated noise stimuli in rat auditory cortex. J Neurosci 31:6414–6420.
41. Moore GP, Segundo JP, Perkel DH, Levitan H (1970) Statistical signs of synaptic interaction in neurons. Biophys J 10:876–900.
42. Nauhaus I, Benucci A, Carandini M, Ringach DL (2008) Neuronal selectivity and local map structureinvisual cortex. Neuron 57:673–679.
43. Okun M, Naim A, Lampl I (2010) The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J Neurosci 30:4440–4448.
44. Okun M, Yger P, Marguet SL, Gerard-Mercier F, Benucci A, Katzner S, Busse L, Carandini M, Harris KD (2012) Population rate dynamics and multi-neuron firing patterns in sensory cortex. J Neurosci 32:17108–17119.
45. Pillow JW, Shlens J, Paninski L, Sher A, Litke AM, Chichilnisky EJ, Simoncelli EP (2008) Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature 454:995–999.
46. Poulet JF, Petersen CC (2008) Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454:881–885.
47. Priebe NJ, Ferster D (2012) Mechanisms of neuronal computation in mammalian visual cortex. Neuron 75:194–208.
48. Reich DS, Victor JD, Knight BW, Ozaki T, Kaplan E (1997) Response variability and timing precision of neuronal spike trains in vivo. J Neuro-physiol 77:2836–2841.
49. 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.
50. Ringach DL (2009) Spontaneous and driven cortical activity: implications for computation. Curr Opin Neurobiol 19:439–444.
51. Ringach DL, Hawken MJ, Shapley R (1997) Dynamics of orientation tuning in macaque primary visual cortex. Nature 387:281–284.
52. Sadagopan S, Ferster D (2012) Feedforward origins of response variability underlying contrast invariant orientation tuning incat visual cortex. Neuron 74:911–923.
53. Saleem AB, Chadderton P, Apergis-Schoute J, Harris KD, Schultz SR (2010) Methods for predicting cortical UP and DOWN states from the phase of deep layer local field potentials. J Comput Neurosci 29:49–62.
54. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870–3896.
55. Smith MA, Kohn A (2008) Spatial and temporal scales of neuronal correlation in primary visual cortex. J Neurosci 28:12591–12603.
56. Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137:1087–1106.
57. Tan AY, Chen Y, Scholl B, Seidemann E, Priebe NJ (2014) Sensory stimulation shifts visual cortex from synchronous to asynchronous states. Nature 509:226–229.
58. Tolhurst DJ, Movshon JA, Dean AF (1983) The statistical reliability of signals insingle neuronsin cat and monkey visual cortex. Vision Res 23:775-785.
59. Truccolo W, Hochberg LR, Donoghue JP (2010) Collective dynamics in human and monkey sensorimotor cortex: predicting single neuron spikes. Nat Neurosci 13:105–111.
60. Ts’o DY, Gilbert CD, Wiesel TN (1986) Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 6:1160–1170.
61. Tsodyks M, Kenet T, Grinvald A, Arieli A (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286:1943–1946.
62. Vogels R, Spileers W, Orban GA (1989) The response variability of striate cortical neurons in the behaving monkey. Exp Brain Res 77:432–436.