Adaptation improves neural coding efficiency despite increasing correlations in variability

Journal of Neuroscience

Volumn 33, Issue 5, 2013, Pages 2108-2120

  Adibi, Mehdi ^a   McDonald, James S ^a   Clifford, Colin W G ^b   Arabzadeh, Ehsan ^a,c  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ELECTRODE; ELECTROPHYSIOLOGY; MALE; NONHUMAN; PERCEPTIVE THRESHOLD; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; RAT; SINGLE UNIT ACTIVITY; SPIKE WAVE; TACTILE DISCRIMINATION; TACTILE STIMULATION; VIBRATION; VIBRATION SENSE; VIBRISSA;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; MALE; NEURONS; PHYSICAL STIMULATION; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 84873044825     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3449-12.2013     Document Type: Article

References (71)

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. Abbott LF, Rajan K, Sompolinsky H (2011) Interactions between intrinsic and stimulus-evoked activity in recurrent neural networks. In: The Dynamic brain: an exploration of neuronal variability and its functional significance (Ding M, Glanzman DL, eds), pp 65-82. New York: Oxford UP.
3. Adibi M, Arabzadeh E (2011) A comparison of neuronal and behavioral detection and discrimination performances in rat whisker system. J Neurophysiol 105:356-365. CrossRef Medline
4. Adibi M, Diamond ME, Arabzadeh E (2012) Behavioral study of whiskermediated vibration sensation in rats. Proc Natl Acad Sci U S A 109:971-976. CrossRef Medline
5. Ahissar E, Knutsen PM (2008) Object localization with whiskers. Biological Cybernetics 98:449-458. CrossRef Medline
6. Arabzadeh E, Petersen RS, Diamond ME (2003) Encoding of whisker vibration by rat barrel cortex neurons: implications for texture discrimination. J Neurosci 23:9146-9154. Medline
7. Arabzadeh E, Panzeri S, Diamond ME (2004) Whisker vibration information carried by rat barrel cortex neurons. J Neurosci 24:6011-6020. CrossRef Medline
8. Arabzadeh E, Zorzin E, Diamond ME (2005) Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol 3:e17. CrossRef Medline
9. Averbeck BB, Lee D (2003) Neural noise and movement-related codes in the macaque supplementary motor area. J Neurosci 23:7630-7641. Medline
10. Averbeck BB, Lee D (2006) Effects of noise correlations on information encoding and decoding. J Neurophysiol 95:3633-3644. CrossRef Medline
11. Averbeck BB, Crowe DA, Chafee MV, Georgopoulos AP (2003) Neural activity in prefrontal cortex during copying geometrical shapes. Exp Brain Res 150:142-153. CrossRef Medline
12. Averbeck BB, Latham PE, Pouget A (2006) Neural correlations, population coding and computation. Nat Rev Neurosci 7:358-366. CrossRef Medline
13. Barlow HB (1961) Possible principles underlying the transformation of sensory messages. In: Sensory Communication (Rosenblith WA, ed), pp 217-234. Cambridge, MA: MIT.
14. Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12:4745-4765. Medline
15. Cafaro J, Rieke F (2010) Noise correlations improve response fidelity and stimulus encoding. Nature 468:964-967. CrossRef Medline
16. Churchland MM, Yu BM, Ryu SI, Santhanam G, Shenoy KV (2006) Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci 26:3697-3712. CrossRef Medline
17. 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
18. Cohen MR, Kohn A (2011) Measuring and interpreting neuronal correlations. Nat Neurosci 14:811-819. CrossRef Medline
19. Cohen MR, Maunsell JHR (2009) Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12:1594-1600. CrossRef Medline
20. Cover TM, Thomas JA (1991) Elements of information theory. New York: Wiley.
21. de la Rocha J, Doiron B, Eric Shea-Brown E, Josić K, Reyes A (2007) Correlation between neural spike trains increases with firing rate. Nature 448: 802-806. CrossRef Medline
22. Dean I, Harper NS, McAlpine D (2005) Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8:1684-1689. CrossRef Medline
23. Diamond ME, Arabzadeh E (2012) Whisker sensory system-from receptor to decision. Prog Neurobiol. Advance online publication. Retrieved June 6, 2012. doi:10.1016/j.pneurobio.2012.05.013. CrossRef Medline
24. Diamond ME, von Heimendahl M, Arabzadeh E (2008a) Whisker-mediated texture discrimination. PloS Biol 6:e220. CrossRef
25. Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E (2008b) Where and what is the whisker sensorimotor system? Nat Rev Neurosci 9:601-612. CrossRef Medline
26. Durant S, Clifford CWG, Crowder NA, Price NSC, Ibbotson MR (2007) Characterizing contrast adaptation in a population of cat primary visual cortical neurons using Fisher information. J Opt Soc Am Opt Image Vis Sci 24:1529-1537. CrossRef Medline
27. Garcia-Lazaro JA, Ho SS, Nair A, Schnupp JW (2007) Shifting and scaling adaptation to dynamic stimuli in somatosensory cortex. Eur J Neurosci 26:2359-2368. CrossRef Medline
28. Gawne TJ, Richmond BJ (1993) How independent are the messages carried by adjacent inferior temporal cortical neurons? J Neurosci 13:2758-2771. Medline
29. Gawne TJ, Kjaer TW, Hertz JA, Richmond BJ (1996) Adjacent visual cortical complex cells share about 20% of their stimulus-related information. Cereb Cortex 6:482-489. CrossRef Medline
30. Ghim JW, Huh N, Jung MW, Oh JH (2008) Information transmission by stimulus-dependent modulation of noise correlation. Neuroreport 19: 453-457. CrossRef Medline
31. Ghim JW, Baeg EH, Kim YB, Jung MW (2011) Stimulus-induced reduction of noise correlation in rat prefrontal cortex. Neuroreport 22:824-829. CrossRef Medline
32. Golledge HDR, Panzeri S, Zheng F, Pola G, Scannell JW, Giannikopoulos DV, Mason RJ, Tovée MJ, Young MP (2003) Correlations, feature-binding and population coding in primary visual cortex. Neuroreport 14:1045-1050. CrossRef Medline
33. Graf ABA, Kohn A, Jazayeri M, Movshon JA (2011) Decoding the activity of neuronal populations in macaque primary visual cortex. Nat Neurosci 14:239-245. CrossRef Medline
34. Gutnisky DA, Dragoi V (2008) Adaptive coding of visual information in neural populations. Nature 452:220-224. CrossRef Medline
35. Hofer SB, Ko H, Pichler B, Vogelstein J, Ros H, Zeng H, Lein E, Lesica NA, Mrsic-Flogel TD (2011) Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat Neurosci 14:1045-1052. CrossRef Medline
36. Hosoya T, Baccus SA, Meister M (2005) Dynamic predictive coding by the retina. Nature 436:71-77. CrossRef Medline
37. Johnson KO (1980) Sensory discrimination: decision process. J Neuro physiol 43:1771-1792. Medline
38. Khatri V, Bruno RM, Simons DJ (2009) Stimulus-specific and stimulusnonspecific firing synchrony and its modulation by sensory adaptation in the whisker-to-barrel pathway. J Neurophysiol 101:2328-2338. CrossRef Medline
39. Kohn A, Smith MA (2005) Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J Neurosci 25:3661-3673. CrossRef Medline
40. Kvale MN, Schreiner CE (2004) Short-term adaptation of auditory receptive fields to dynamic stimuli. J Neurophysiol 91:604-612. CrossRef Medline
41. Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36-41. CrossRef Medline
42. Magri C, Whittingstall K, Singh V, Logothetis NK, Panzeri S (2009) A toolbox for the fast information analysis of multiple-site LFP, EEG and spike train recordings. BMC Neurosci 10:81. CrossRef Medline
43. Maravall M, Petersen RS, Fairhall AL, Arabzadeh E, Diamond ME (2007) Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biol 5:e19. CrossRef Medline
44. Nagel KI, Doupe AJ (2006) Temporal processing and adaptation in the songbird auditory forebrain. Neuron 51:845-859. CrossRef Medline
45. Nemenman I, Bialek W, Van Steveninck RR (2004) Entropy and information in neural spike trains: Progress on the sampling problem. Phys Rev E Stat Nonlin Soft Matter Phys 69:056111. CrossRef Medline
46. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792-1804. CrossRef Medline
47. Oram MW (2011) Visual stimulation decorrelates neuronal activity. J Neurophysiol 105:942-957. CrossRef Medline
48. Oram MW, Földiák P, Perrett DI, Sengpiel F (1998) The 'Ideal Homunculus': decoding neural population signals. Trends Neurosci 21:259-265. CrossRef Medline
49. Osborne LC, Bialek W, Lisberger SG (2004) Time course of information about motion direction in visual area MT of macaque monkeys. J Neurosci 24:3210-3222. CrossRef Medline
50. Panzeri S, Treves A (1996) Analytical estimates of limited sampling biases in different information measures. Network 7:87-107. CrossRef
51. Panzeri S, Schultz SR, Treves A, Rolls ET (1999) Correlations and the encoding of information in the nervous system. Proc R Soc Lond B Biol Sci 266:1001-1012. CrossRef Medline
52. Panzeri S, Senatore R, Montemurro MA, Petersen RS (2007) Correcting for the sampling bias problem in spike train information measures. J Neurophysiol 98:1064-1072. CrossRef Medline
53. Pearson KFRS (1901) LIII. On lines and planes of closest fit to systems of points in space. The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science 2:559-572.
54. Petersen RS, Panzeri S, Diamond ME (2001) Population coding of stimulus location in rat somatosensory cortex. Neuron 32:503-514. CrossRef Medline
55. 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. CrossRef Medline
56. Price NSC, Ono S, Mustari MJ, Ibbotson MR (2005) Comparing acceleration and speed tuning in macaque MT: physiology and modeling. J Neurophysiol 94:3451-3464. CrossRef Medline
57. Reich DS, Mechler F, Victor JD (2001) Independent and redundant information in nearby cortical neurons. Science 294:2566-2568. CrossRef 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. CrossRef Medline
59. Rolls ET, Franco L, Aggelopoulos NC, Reece S (2003) An information theoretic approach to the contributions of the firing rates and the correlations between the firing of neurons. J Neurophysiol 89:2810-2822. CrossRef Medline
60. Romo R, Hernández A, Zainos A, Salinas E (2003) Correlated neuronal discharges that increase coding efficiency during perceptual discrimination. Neuron 38:649-657. CrossRef Medline
61. Schneidman E, Berry MJ 2nd, Segev R, Bialek W (2006) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440:1007-1012. CrossRef Medline
62. Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M (1997) Adaptation of retinal processing to image contrast and spatial scale. Nature 386:69-73. CrossRef Medline
63. Smith MA, Kohn A (2008) Spatial and temporal scales of neuronal correlation in primary visual cortex. J Neurosci 28:12591-12603. CrossRef Medline
64. Sommerville DMY (1958) An introduction to the geometry of n dimensions. New York: Dover.
65. Sompolinsky H, Yoon H, Kang K, Shamir M (2001) Population coding in neuronal systems with correlated noise. Phys Rev E Stat Nonlin Soft Matter Phys 64:051904. CrossRef Medline
66. Strong SP, Koberle R, de Ruyter van Steveninck RR, Bialek W (1998) Entropy and information in neural spike trains. Phys Rev Lett 80:197-200. CrossRef
67. Uka T, DeAngelis GC (2003) Contribution of middle temporal area to coarse depth discrimination: comparison of neuronal and psychophysical sensitivity. J Neurosci 23:3515-3530. Medline
68. Wen B, Wang GI, Dean I, Delgutte B (2009) Dynamic range adaptation to sound level statistics in the auditory nerve. J Neurosci 29:13797-13808. CrossRef Medline
69. Wilke SD, Eurich CW (2002) Representational accuracy of stochastic neural populations. Neural Comput 14:155-189. CrossRef Medline
70. Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242. CrossRef Medline
71. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140-143. CrossRef Medline