Measuring and interpreting neuronal correlations

Nature Neuroscience

Volumn 14, Issue 7, 2011, Pages 811-819

  Cohen, Marlene R ^a   Kohn, Adam ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN CORTEX; BRAIN FUNCTION; BRAIN NERVE CELL; CORRELATION ANALYSIS; HUMAN; NERVE CELL NETWORK; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIMULATION;

ACTION POTENTIALS; ANIMALS; CELL COMMUNICATION; CEREBRAL CORTEX; HUMANS; MODELS, NEUROLOGICAL; MODELS, STATISTICAL; NEURONS;

EID: 79959663278     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2842     Document Type: Review

References (92)

1. Tolhurst, D.J., Movshon, J.A. & Dean, A.F. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res. 23, 775-785 (1983). (Pubitemid 13035193)
2. Shadlen, M.N. & Newsome, W.T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870-3896 (1998). (Pubitemid 28225693)
3. Abbott, L.F. & Dayan, P. The effect of correlated variability on the accuracy of a population code. Neural Comput. 11, 91-101 (1999).
4. Averbeck, B.B., Latham, P.E. & Pouget, A. Neural correlations, population coding and computation. Nat. Rev. Neurosci. 7, 358-366 (2006).
5. Nirenberg, S. & Latham, P.E. Decoding neuronal spike trains: how important are correlations? Proc. Natl. Acad. Sci. USA 100, 7348-7353 (2003). (Pubitemid 36712193)
6. Zohary, E., Shadlen, M.N. & Newsome, W.T. Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370, 140-143 (1994). (Pubitemid 24229125)
7. Cohen, M.R. & Maunsell, J.H. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12, 1594-1600 (2009).
8. Mitchell, J.F., Sundberg, K.A. & Reynolds, J.H. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63, 879-888 (2009).
9. Aertsen, A.M., Gerstein, G.L., Habib, M.K. & Palm, G. Dynamics of neuronal firing correlation: modulation of "effective connectivity". J. Neurophysiol. 61, 900-917 (1989).
10. Ahissar, E. et al. Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. Science 257, 1412-1415 (1992).
11. Espinosa, I.E. & Gerstein, G.L. Cortical auditory neuron interactions during presentation of 3-tone sequences: effective connectivity. Brain Res. 450, 39-50 (1988).
12. Kohn, A. & Smith, M.A. Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J. Neurosci. 25, 3661-3673 (2005).
13. Gutnisky, D.A. & Dragoi, V. Adaptive coding of visual information in neural populations. Nature 452, 220-224 (2008). (Pubitemid 351380238)
14. Komiyama, T. et al. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464, 1182-1186 (2010).
15. Cohen, M.R. & Newsome, W.T. Context-dependent changes in functional circuitry in visual area MT. Neuron 60, 162-173 (2008).
16. Poulet, J.F. & Petersen, C.C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881-885 (2008).
17. Vaadia, E. et al. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373, 515-518 (1995).
18. Seriès, P., Latham, P.E. & Pouget, A. Tuning curve sharpening for orientation selectivity: coding efficiency and the impact of correlations. Nat. Neurosci. 7, 1129-1135 (2004). (Pubitemid 41184454)
19. Greschner, M. et al. Correlated firing among major ganglion cell types in primate retina. J. Physiol. (Lond.) 589, 75-86 (2011).
20. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281-284 (1995).
21. Alonso, J.M. & Martinez, L.M. Functional connectivity between simple cells and complex cells in cat striate cortex. Nat. Neurosci. 1, 395-403 (1998).
22. Bair, W., Zohary, E. & Newsome, W.T. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J. Neurosci. 21, 1676-1697 (2001). (Pubitemid 32182208)
23. Reich, D.S., Mechler, F. & Victor, J.D. Independent and redundant information in nearby cortical neurons. Science 294, 2566-2568 (2001). (Pubitemid 34027300)
24. Constantinidis, C. & Goldman-Rakic, P.S. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J. Neurophysiol. 88, 3487-3497 (2002). (Pubitemid 35448724)
25. Lee, D., Port, N.L., Kruse, W. & Georgopoulos, A.P. Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex. J. Neurosci. 18, 1161-1170 (1998). (Pubitemid 28112937)
26. Smith, M.A. & Kohn, A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28, 12591-12603 (2008).
27. Averbeck, B.B. & Lee, D. Neural noise and movement-related codes in the macaque supplementary motor area. J. Neurosci. 23, 7630-7641 (2003). (Pubitemid 37034080)
28. Ecker, A.S. et al. Decorrelated neuronal firing in cortical microcircuits. Science 327, 584-587 (2010).
29. Huang, X. & Lisberger, S.G. Noise correlations in cortical area MT and their potential impact on trial-by-trial variation in the direction and speed of smooth-pursuit eye movements. J. Neurophysiol. 101, 3012-3030 (2009).
30. Jermakowicz, W.J., Chen, X., Khaytin, I., Bonds, A.B. & Casagrande, V.A. Relationship between spontaneous and evoked spike-time correlations in primate visual cortex. J. Neurophysiol. 101, 2279-2289 (2009).
31. Rasch, M.J., Schuch, K., Logothetis, N.K. & Maass, W. Statistical comparison of spike responses to natural stimuli in monkey area V1 with simulated responses of a detailed laminar network model for a patch of V1. J. Neurophysiol. 105, 757-778 (2011).
32. Zhang, M. & Alloway, K.D. Stimulus-induced intercolumnar synchronization of neuronal activity in rat barrel cortex: a laminar analysis. J. Neurophysiol. 92, 1464-1478 (2004). (Pubitemid 39100646)
33. Renart, A. et al. The asynchronous state in cortical circuits. Science 327, 587-590 (2010).
34. de la Rocha, J., Doiron, B., Shea-Brown, E., Josic, K. & Reyes, A. Correlation between neural spike trains increases with firing rate. Nature 448, 802-806 (2007). (Pubitemid 47266336)
35. Lampl, I., Reichova, I. & Ferster, D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22, 361-374 (1999). (Pubitemid 29109669)
36. Okun, M. & Lampl, I. Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat. Neurosci. 11, 535-537 (2008). (Pubitemid 351595199)
37. Kazama, H. & Wilson, R.I. Origins of correlated activity in an olfactory circuit. Nat. Neurosci. 12, 1136-1144 (2009).
38. Dorn, J.D. & Ringach, D.L. Estimating membrane voltage correlations from extracellular spike trains. J. Neurophysiol. 89, 2271-2278 (2003). (Pubitemid 36444279)
39. Carandini, M. Amplification of trial-to-trial response variability by neurons in visual cortex. PLoS Biol. 2, e264 (2004).
40. Mazurek, M.E. & Shadlen, M.N. Limits to the temporal fidelity of cortical spike rate signals. Nat. Neurosci. 5, 463-471 (2002). (Pubitemid 34454253)
41. Bedenbaugh, P. & Gerstein, G.L. Multiunit normalized cross correlation differs from the average single-unit normalized correlation. Neural Comput. 9, 1265-1275 (1997). (Pubitemid 127469148)
42. Rosenbaum, R.J., Trousdale, J. & Josic, K. Pooling and correlated neural activity. Front. Comput. Neurosci. 4, 9 (2010).
43. Müller, H.J. & Rabbitt, P.M. Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J. Exp. Psychol. Hum. Percept. Perform. 15, 315-330 (1989).
44. Cheal, M. & Lyon, D.R. Central and peripheral precuing of forced-choice discrimination. Q. J. Exp. Psychol. A 43, 859-880 (1991).
45. Müller, M.M., Teder-Salejarvi, W. & Hillyard, S.A. The time course of cortical facilitation during cued shifts of spatial attention. Nat. Neurosci. 1, 631-634 (1998).
46. Kröse, B.J. & Julesz, B. The control and speed of shifts of attention. Vision Res. 29, 1607-1619 (1989). (Pubitemid 19263054)
47. Nakayama, K. & Mackeben, M. Sustained and transient components of focal visual attention. Vision Res. 29, 1631-1647 (1989). (Pubitemid 19263056)
48. Bisley, J.W. & Goldberg, M.E. Neuronal activity in the lateral intraparietal area and spatial attention. Science 299, 81-86 (2003). (Pubitemid 36042404)
49. Herrington, T.M. & Assad, J.A. Neural activity in the middle temporal area and lateral intraparietal area during endogenously cued shifts of attention. J. Neurosci. 29, 14160-14176 (2009).
50. Bair, W. & O'Keefe, L.P. The influence of fixational eye movements on the response of neurons in area MT of the macaque. Vis. Neurosci. 15, 779-786 (1998). (Pubitemid 28358391)
51. Berens, P., Keliris, G.A., Ecker, A.S., Logothetis, N.K. & Tolias, A.S. Feature selectivity of the gamma-band of the local field potential in primate primary visual cortex. Front. Neurosci. 2, 199-207 (2008).
52. Amari, S. Measure of correlation orthogonal to change in firing rate. Neural Comput. 21, 960-972 (2009).
53. Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87-100 (1996). (Pubitemid 3026944)
54. Nienborg, H. & Cumming, B. Correlations between the activity of sensory neurons and behavior: how much do they tell us about a neuron's causality? Curr. Opin. Neurobiol. 20, 376-381 (2010).
55. Parker, A.J. & Newsome, W.T. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21, 227-277 (1998). (Pubitemid 28150664)
56. Palmer, C., Cheng, S.Y. & Seidemann, E. Linking neuronal and behavioral performance in a reaction-time visual detection task. J. Neurosci. 27, 8122-8137 (2007). (Pubitemid 47173322)
57. Bollimunta, A., Chen, Y., Schroeder, C.E. & Ding, M. Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques. J. Neurosci. 28, 9976-9988 (2008).
58. Thut, G., Nietzel, A., Brandt, S.A. & Pascual-Leone, A. Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J. Neurosci. 26, 9494-9502 (2006). (Pubitemid 44396862)
59. Fox, M.D., Snyder, A.Z., Vincent, J.L. & Raichle, M.E. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 56, 171-184 (2007). (Pubitemid 47484178)
60. Grill-Spector, K., Knouf, N. & Kanwisher, N. The fusiform face area subserves face perception, not generic within-category identification. Nat. Neurosci. 7, 555-562 (2004). (Pubitemid 38544596)
61. Leber, A.B. Neural predictors of within-subject fluctuations in attentional control. J. Neurosci. 30, 11458-11465 (2010).
62. Ress, D., Backus, B.T. & Heeger, D.J. Activity in primary visual cortex predicts performance in a visual detection task. Nat. Neurosci. 3, 940-945 (2000).
63. Ress, D. & Heeger, D.J. Neuronal correlates of perception in early visual cortex. Nat. Neurosci. 6, 414-420 (2003). (Pubitemid 36373988)
64. Sapir, A., d'Avossa, G., McAvoy, M., Shulman, G.L. & Corbetta, M. Brain signals for spatial attention predict performance in a motion discrimination task. Proc. Natl. Acad. Sci. USA 102, 17810-17815 (2005). (Pubitemid 41803579)
65. Nienborg, H. & Cumming, B.G. Decision-related activity in sensory neurons reflects more than a neuron's causal effect. Nature 459, 89-92 (2009).
66. Cohen, M.R. & Newsome, W.T. Estimates of the contribution of single neurons to perception depend on timescale and noise correlation. J. Neurosci. 29, 6635-6648 (2009).
67. Cook, E.P. & Maunsell, J.H. Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nat. Neurosci. 5, 985-994 (2002).
68. Price, N.S. & Born, R.T. Timescales of sensory-and decision-related activity in the middle temporal and medial superior temporal areas. J. Neurosci. 30, 14036-14045 (2010).
69. Ditterich, J., Mazurek, M.E. & Shadlen, M.N. Microstimulation of visual cortex affects the speed of perceptual decisions. Nat. Neurosci. 6, 891-898 (2003). (Pubitemid 36929712)
70. Huk, A.C. & Shadlen, M.N. Neural activity in macaque parietal cortex reflects temporal integration of visual motion signals during perceptual decision making. J. Neurosci. 25, 10420-10436 (2005). (Pubitemid 41628446)
71. Beck, J.M. et al. Probabilistic population codes for Bayesian decision making. Neuron 60, 1142-1152 (2008).
72. Mazurek, M.E., Roitman, J.D., Ditterich, J. & Shadlen, M.N. A role for neural integrators in perceptual decision making. Cereb. Cortex 13, 1257-1269 (2003). (Pubitemid 37323002)
73. Wang, X.J. Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36, 955-968 (2002).
74. Wong, K.F., Huk, A.C., Shadlen, M.N. & Wang, X.J. Neural circuit dynamics underlying accumulation of time-varying evidence during perceptual decision making. Front. Comput. Neurosci. 1, 6 (2007).
75. Truccolo, W., Eden, U.T., Fellows, M.R., Donoghue, J.P. & Brown, E.N. A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. J. Neurophysiol. 93, 1074-1089 (2005).
76. Kass, R.E., Ventura, V. & Brown, E.N. Statistical issues in the analysis of neuronal data. J. Neurophysiol. 94, 8-25 (2005). (Pubitemid 40923224)
77. Paninski, L. et al. A new look at state-space models for neural data. J. Comput. Neurosci. 29, 107-126 (2010).
78. Okatan, M., Wilson, M.A. & Brown, E.N. Analyzing functional connectivity using a network likelihood model of ensemble neural spiking activity. Neural Comput. 17, 1927-1961 (2005). (Pubitemid 41057057)
79. Pillow, J.W. et al. Spatio-temporal correlations and visual signaling in a complete neuronal population. Nature 454, 995-999 (2008).
80. Truccolo, W., Hochberg, L.R. & Donoghue, J.P. Collective dynamics in human and monkey sensorimotor cortex: predicting single neuron spikes. Nat. Neurosci. 13, 105-111 (2010).
81. Kohn, A., Zandvakili, A. & Smith, M.A. Correlations and brain states: from electrophysiology to functional imaging. Curr. Opin. Neurobiol. 19, 434-438 (2009).
82. Poort, J. & Roelfsema, P.R. Noise correlations have little influence on the coding of selective attention in area V1. Cereb. Cortex 19, 543-553 (2009).
83. Samonds, J.M., Potetz, B.R. & Lee, T.S. Cooperative and competitive interactions facilitate stereo computations in macaque primary visual cortex. J. Neurosci. 29, 15780-15795 (2009).
84. Erickson, C.A., Jagadeesh, B. & Desimone, R. Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys. Nat. Neurosci. 3, 1143-1148 (2000).
85. Averbeck, B.B. & Lee, D. Effects of noise correlations on information encoding and decoding. J. Neurophysiol. 95, 3633-3644 (2006). (Pubitemid 43846170)
86. Stark, E., Globerson, A., Asher, I. & Abeles, M. Correlations between groups of premotor neurons carry information about prehension. J. Neurosci. 28, 10618-10630 (2008).
87. Maynard, E.M. et al. Neuronal interactions improve cortical population coding of movement direction. J. Neurosci. 19, 8083-8093 (1999). (Pubitemid 30225804)
88. Nevet, A., Morris, G., Saban, G., Arkadir, D. & Bergman, H. Lack of spike-count and spike-time correlations in the substantia nigra reticulata despite overlap of neural responses. J. Neurophysiol. 98, 2232-2243 (2007). (Pubitemid 47584408)
89. Cohen, J.Y. et al. Cooperation and competition among frontal eye field neurons during visual target selection. J. Neurosci. 30, 3227-3238 (2010).
90. Bichot, N.P., Thompson, K.G., Chenchal Rao, S. & Schall, J.D. Reliability of macaque frontal eye field neurons signaling saccade targets during visual search. J. Neurosci. 21, 713-725 (2001). (Pubitemid 32107459)
91. Barlow, H.B. & Foldiak, P. Adaptation and decorrelation in the cortex. in The Computing Neuron (eds. Durbin, R., Miall, C. & Mitchinson, G.) (Addison-Wesley, New York, 1989).
92. Vinje, W.E. & Gallant, J.L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273-1276 (2000). (Pubitemid 30112150)