The role of correlations in direction and contrast coding in the primary visual cortex

Journal of Neuroscience

Volumn 27, Issue 9, 2007, Pages 2338-2348

  Montani, Fernando ^a   Kohn, Adam ^b,c   Smith, Matthew A ^b,d   Schultz, Simon R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NEW YORK UNIVERSITY   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Cerebral cortex; Extracellular recording; Information theory; Neuronal ensembles; Redundancy; Striate cortex; Synchronization; Synchrony; Synergy

Indexed keywords

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICAL SYNCHRONIZATION; INFORMATION SCIENCE; MACACA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; STIMULUS RESPONSE; VISION; VISUAL CORTEX; VISUAL STIMULATION;

ANIMALS; CORTICAL SYNCHRONIZATION; MACACA FASCICULARIS; MACACA RADIATA; MALE; NEURONS; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 33847346389     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3417-06.2007     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.
2. Averbeck BB, Lee D (2003) Neural noise and movement-related codes in the macaque supplement area. J Neurosci 23:7630-7641.
3. Averbeck BB, Lathan PE, Pouget A (2006) Neural correlations, population coding and computation. Nat Rev Neurosci 7:358-366.
4. Bair W, Zohary E, Newsome WT (2001) Correlated firing in macaque visual area MT: time scales and relationship to behavior. J Neurosci 21:1676-1697.
5. Cavanaugh JR, Bair W, Movshon JA (2002) Nature and interaction of signals from the receptive field enter and surround in macaque V1. J Neurophysiol 88:2530-2546.
6. Cover TM, Thomas JA Elements of information theory. New York: Wiley.
7. Dan Y, Alonso J-M, Usrey WM, Reid RC (1998) Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat Neurosci 1:501-507.
8. Das A, Gilbert CD 1999 Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399:655-661.
9. De Angelis GC, Ghose GM, Ohzawa I, Freeman RD (1999) Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons. J Neurosci 19:4046-4064.
10. De Charms RC, Merzenich MM (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381:610-613.
11. De Oliveira SC, Thiele A, Hoffman KP (1997) Synchronization of neural activity during stimulus expectation in a direction discrimination task. J Neurosci 17:9248-9260.
12. Engel AK, König P, Gray CM, Singer W (1990) Stimulus-dependent neuronal oscillations in cat visual cortex: inter-columnar interactions as determined by cross-correlation analysis. Biol Cybern 60:121-130.
13. Gawne TJ, Richmond BJ (1993) How independent are the messages carried by adjacent inferior temporal cortical neurons? J Neurosci 13:2758-2771.
14. Gawne TJ, Kjaer TW, Herz JA, Richmond BJ (1996) Adjacent visual cortical complex cells share about 20% of their stimulus-related information. Cereb Cortex 6:482-489.
15. Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 243:1416-1419.
16. Golledge HD, Panzeri S, Zheng F, Pola G, Scannell JW, Giannikopoulos DV, Mason RJ, Tovee MJ, Young MP (2003) Correlations, feature-binding and population coding in primary visual cortex. NeuroReport 14:1045-1050.
17. Gray CM (1999) The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24:31-47.
18. Häusser M, Mel B (2003) Dendrites: bug or feature? Curr Opin Neurobiol 13:372-383.
19. Imas OA, Ropella KM, Wood JD, Hudetz AG (2004) Halothane augments event-related gamma oscillations in rat visual cortex. Neuroscience 123:269-278.
20. Kayser C, Konig P (2004) Population coding of orientation in the visual cortex of alert cats - an information theoretic analysis. NeuroReport 15:2761-2764.
21. Kohn A, Smith MA (2005) Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J Neurosci 25:3661-3673.
22. Kreiter AK, Singer W (1992) Oscillatory neuronal responses in the visual cortex of awake macaque monkey. Eur J Neurosci 4:369 -375.
23. Kreiter AK, Singer W (1996) Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J Neurosci 16:2381-2396.
24. Latham PE, Nirenberg S (2005) Synergy, redundancy, and independence in population codes, revisited. J Neurosci 25:5195-5206.
25. Lebedev MA, Mirabella G, Erchova I, Diamond ME (2000) Experience dependence plasticity of rat barrel cortex: redistribution of activity across barrel-columns. Cereb Cortex 10:23-31.
26. Lee D, Port NL, Kruse W, Georgopoulus AP (1998) Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex. J Neurosci 18:1161-1170.
27. Maldonado PE, Friedman-Hill S, Gray CM (2000) Dynamics of striate cortical activity in the alert macaque. II. Fast time scale synchronization. Cereb Cortex 10:1117-1131.
28. Mastronarde DN (1983) Correlated firing of cat retinal ganglion cells. I. Spontaneously active input to X- and Y-cells. J Neurophysiol 49:303-324.
29. Mazurek ME, Shadlen MN (2002) Limits to the temporal fidelity of cortical spike rate signals. Nat Neurosci 5:463-471.
30. Meister M (1996) Multineuronal codes in retinal signaling. Proc Natl Acad Sci USA 93:609-614.
31. Movshon JA, Albright TD, Stoner GR, Majaj NJ, Smith MA (2003) Cortical responses to visual motion in alert and anesthetized monkeys. Nat Neurosci 6:3.
32. Nelson JI, Salin PA, Munk MH-J, Bullier J (1992) Spatial and temporal coherence in cortico-cortical connections: a cross-correlation study in areas 17-18 in the cat. Vis Neurosci 9:21-37.
33. Nemenman I, Shafee F, Bialek W (2002) Entropy and inference, revisited. In: Advances in neural information processing 14 (Dietterich TG, Becker S, Ghahramani Z, eds). Cambridge, MA: MIT.
34. Nemenman I, Bialek W, de Ruyter van Steveninck R (2004) Entropy and information in neuronal spike trains: progress on the sampling problem (E-pub). Phys Rev E Stat Nonlin Soft Matter Phys 69:056111.
35. Nirenberg S, Latham PE (2003) Decoding neuronal spike trains: how important are correlations? Proc Natl Acad Sci USA 100:7348-7353.
36. Nirenberg S, Carcieri SM, Jacobs AL, Latham PE (2001) Retinal ganglion cells act largely as independent encoders. Nature 411:698-701.
37. Nowak LG, Munk MHJ, James AC, Girard P, Bullier J (1999) Cross correlation study of the temporal interactions between areas V1 and V2 of the macaque monkey. J Neurophysiol 81:1057-1074.
38. Oram MW, Hatsopoulos NG, Richmond BJ, Donoghue JP (2001) Excess synchrony in motor cortical neurons provides redundant direction information with that from coarse temporal measures. J Neurophysiol 86:1700-1716.
39. Panzeri S, Schultz SR (2001) A unified approach to the study of temporal, correlational, and rate coding. Neural Comput 13:1311-1349.
40. Panzeri S, Treves A (1996) Analytical estimates of limited sampling biases in different information measures. Network 7:87-107.
41. 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.
42. Panzeri S, Petersen SR, Schultz SR, Lebedev M, Diamond M (2001) The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29:769-777.
43. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7:419-440.
44. Petersen RS, Panzeri S, Diamond ME (2001) Population coding of stimulus location in rat somatosensory cortex. Neuron 32:503-514.
45. Pola G, Thiele A, Hoffmann K-P, Panzeri S (2003) An exact method to quantify the information transmitted by different mechanisms of correlational coding. Network 14:35-60.
46. Puchalla JL, Schneidman E, Harris RA, Berry MJ (2005) Redundancy in the population code of the retina. Neuron 46:493-504.
47. Reich DS, Mechler F, Victor JD (2001) Independent and redundant information in nearby cortical neurons. Science 294:2566-2568.
48. Richmond BJ, Gawne TJ (1998) The relationship between neuronal codes and cortical organization. In: Neuronal ensembles, strategies for recording and decoding (Eichenbaum HB, Davis JL, eds), pp 57-79. New York: Wiley.
49. Roelfsema PR, Engel AK, Koenig P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157-161.
50. Samonds JM, Bonds AB (2005) Gamma oscillation maintains stimulus structure-dependent synchronization in cat visual cortex. J Neurophysiol 93:223-236.
51. Samonds JM, Allison JD, Brown HA, Bonds AB (2003) Cooperation between area 17 neuron pairs enhances fine discrimination of orientation. J Neurosci 23:2416-2425.
52. Samonds JM, Allison JD, Brown HA, Bonds AB (2004) Cooperative synchronized assemblies enhance orientation discrimination. Proc Natl Acad Sci USA 101:6722-6727.
53. Samonds JM, Zhou Z, Bernard MR, Bonds AB (2006) Synchronous activity in cat visual cortex encodes collinear and cocircular contours. J Neurophysiol 95:2602-2616.
54. Schneidman E, Bialek W, Berry MJ (2003) Synergy, redundancy, and independence in population codes. J Neurosci 23:11539-11553.
55. Schneidman E, Berry MJ, Segev R, Bialek W (2006) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440:1007-1012.
56. Schultz SR, Panzeri S (2001) Temporal correlations and neural spike train entropy. Phys Rev Lett 86:5823-5826.
57. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
58. Shamir M, Sompolinsky H (2004) Nonlinear population codes. Neural Comput 16:1105-1136.
59. Shannon CE (1948) A mathematical theory of communication. Bell System Tech J 27:379-423.
60. Shlens J, Field G, Gauthier J, Grivich M, Petrusca D, Sher A, Litke A, Chichilnisky EJ (2006) The structure of multi-neuron firing patterns in primate retina. J Neurosci 26:8254-8266.
61. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555-586.
62. Tolhurst DJ (1989) The amount of information transmitted about contrast by neurons in cat's visual cortex. Vis Neurosci 2:409-413.
63. Ts'o DY, Gilbert C (1988) The organization of chromatic and spatial interactions in the primate striate cortex. J Neurosci 8:1712-1727.
64. Werner G, Mountcastle VB (1965) Neural activity in mechanoreceptive cutaneous afferents: stimulus-response relations, Weber functions, and information transmission. J Neurophysiol 28:359-397.
65. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140-143.