Shared sensory estimates for human motion perception and pursuit eye movements

Journal of Neuroscience

Volumn 35, Issue 22, 2015, Pages 8515-8530

  Mukherjee, Trishna ^a   Battifarano, Matthew ^a   Simoncini, Claudio ^a   Osborne, Leslie C ^a,b  

^a THE UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Extrastriate cortex; Motor noise; Oculomotor system; Perceptual threshold; Sensory discrimination; Smooth pursuit

Indexed keywords

ARTICLE; EXTRASTRIATE BODY AREA; EYE ACCELERATION; FEMALE; HUMAN; MALE; MOVEMENT PERCEPTION; OCULOMOTOR SYSTEM; OPTIC FLOW; PERCEPTIVE DISCRIMINATION; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; RETINA IMAGE; SENSORY SYSTEM PARAMETERS; SIGNAL NOISE RATIO; SMOOTH PURSUIT EYE MOVEMENT; VISUAL CORTEX; VISUAL STIMULATION; ADULT; EYE MOVEMENT; ORIENTATION; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; PSYCHOPHYSICS; STATISTICS;

ADULT; DISCRIMINATION (PSYCHOLOGY); EYE MOVEMENTS; FEMALE; HUMANS; MALE; MOTION PERCEPTION; OPTIC FLOW; ORIENTATION; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; PSYCHOPHYSICS; SENSORY THRESHOLDS; STATISTICS AS TOPIC;

EID: 84930461726     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4320-14.2015     Document Type: Article

References (75)

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. Averbeck BB, Latham PE, Pouget A (2006) Neural correlations, population coding and computation. Nat Rev Neurosci 7:358-366. CrossRef Medline
3. Born RT, Groh JM, Zhao R, Lukasewycz SJ (2000) Segregation of object and background motion in visual area MT: effects of microstimulation on eye movements. Neuron 26:725–734. CrossRef Medline
4. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA (1996) A Relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis Neurosci 13:87–100. CrossRef Medline
5. Churchland MM, Lisberger SG (2001) Shifts in the population response in the middle temporal visual area parallel perceptual and motor illusions produced by apparent motion. J Neurosci 21:9387–9402. Medline
6. Cohen MR, Kohn A (2011) Measuring and interpreting neuronal correlations. Nat Neurosci 14:811-819. CrossRef Medline
7. De Bruyn B, Orban GA (1988) Human velocity and direction discrimination measured with random dot patterns. Vision Res 28:1323–1335. CrossRef Medline
8. Finney DJ (1971) Probit analysis. London: Cambridge University.
9. Gegenfurtner KR, Xing D, Scott BH, Hawken MJ (2003) A comparison of pursuit eye movement and perceptual performance in speed discrimination. J Vis 3:865-876. Medline
10. Gegenfurtner K, Henriques D, Krauzlis R (2011) Recent advances in perception and action. Vision Res 51:801-803. CrossRef Medline
11. Graf AB, 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
12. Groh JM, Born RT, Newsome WT (1997) How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. J Neurosci 17:4312-4330. Medline
13. Guo CC, Raymond JL (2010) Motor learning reduces eye movement variability through reweighting of sensory inputs. J Neurosci 30:16241-16248. CrossRef Medline
14. Heinen SJ, Watamaniuk SN (1998) Spatial integration in human smooth pursuit. Vision Res 38:3785–3794. CrossRef Medline
15. Hohl SS, Chaisanguanthum KS, Lisberger SG (2013) Sensory population decoding for visually guided movements. Neuron 79:167–179. CrossRef Medline
16. Huang X, Lisberger SG (2009) 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. CrossRef Medline
17. Ilg UJ, Thier P (2008) The neural basis of smooth pursuit eye movements in the rhesus monkey brain. Brain Cogn 68:229-240. CrossRef Medline
18. Joshua M, Lisberger SG (2014) A framework for using signal, noise, and variation to determine whether the brain controls movement synergies or single muscles. J Neurophysiol 111:733–745. CrossRef Medline
19. Komatsu H, Wurtz RH (1988) Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. J Neurophysiol 60:580–603. Medline
20. Komatsu H, Wurtz RH (1989) Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J Neurophysiol 62:31-47. Medline
21. Kowler E, McKee SP (1987) Sensitivity of smooth eye movement to small differences in target velocity. Vision Res 27:993–1015. CrossRef Medline
22. Krauzlis RJ (2004) Recasting the smooth pursuit eye movement system. J Neurophysiol 91:591-603. Medline
23. Krauzlis RJ, Lisberger SG (1994) Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. J Neurophysiol 72:150-162. Medline
24. Krukowski AE, Stone LS (2005) Expansion of direction space around the cardinal axes revealed by smooth pursuit eye movements. Neuron 45: 315–323. CrossRef Medline
25. Leon PS, Vanzetta I, Masson GS, Perrinet LU (2012) Motion Clouds: Model-based stimulus synthesis of natural-like random textures for the study of motion perception. J Neurophysiol 107:3217–3226. CrossRef Medline
26. Lieberman HR (1983) Computation of psychophysical thresholds using the probit technique. Behavior Research Methods and Instrumentation 15: 446–448.
27. CrossRef Lisberger SG (2010) Visual guidance of smooth pursuit eye movements: sensation, action, and what happens in between. Neuron 66:477-491. CrossRef Medline
28. Lisberger SG, Movshon JA (1999) Visual motion analysis for pursuit eye movements in area MT of macaque monkeys. J Neurosci 19:2224-2246. Medline
29. Lisberger SG, Westbrook LE (1985) Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. J Neurosci 5:1662–1673. Medline
30. Lisberger SG, Morris EJ, Tychsen L (1987) Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annu Rev Neurosci 10:97–129. CrossRef Medline
31. Liston DB, Stone LS (2008) Effects of prior information and reward on oculomotor and perceptual choices. J Neurosci 28:13866-13875. CrossRef Medline
32. Liu J, Newsome WT (2003) Functional organization of speed tuned neurons in visual area MT. J Neurophysiol 89:246-256. Medline
33. Liu J, Newsome WT (2005) Correlation between speed perception and neural activity in the middle temporal visual area. J Neurosci 25:711–722. CrossRef Medline
34. Maunsell JH, Van Essen DC (1983) Functional properties of neurons in the middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed and orientations. J Neurophysiol 49:1127–1147. Medline
35. McKee SP, Nakayama K (1984) The detection of motion in the peripheral visual field. Vision Res 24:25–32. CrossRef Medline
36. McKee SP, Klein SA, Teller DY (1985) Statistical properties of forced-choice psychometric functions: Implications of probit analysis. Perception and Psychophysics 37:286-298. CrossRef Medline
37. Medina JF, Lisberger SG (2007) Variation, signal, and noise in cerebellar sensory-motor processing for smooth-pursuit eye movements. J Neurosci 27:6832-6842. CrossRef Medline
38. Milner AD, Goodale MA (2006) The visual brain in action. New York: OUP.
39. Mustari MJ, Ono S, Das VE (2009) Signal processing and distribution in cortical-brainstem pathways for smooth pursuit eye movements. Ann N Y Acad Sci 1164:147–1154. CrossRef Medline
40. Newsome WT, Pare´ EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211. Medline
41. Newsome WT, Wurtz RH, Dürsteler MR, Mikami A (1985) Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. J Neurosci 5:825-840. Medline
42. Newsome WT, Wurtz RH, Komatsu H (1988) Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J Neurophysiol 60:604–620. Medline
43. Newsome WT, Britten KH, Movshon JA (1989) Neuronal correlates of a perceptual decision. Nature 341:52–54. CrossRef Medline
44. Nover H, Anderson CH, DeAngelis GC (2005) A Logarithmic, scale-invariant representation of speed in macaque middle temporal area accounts for speed discrimination performance. J Neurosci 25:10049–10060. CrossRef Medline
45. O’Leary JG, Lisberger SG (2012) Role of the lateral intraparietal area in modulation of the strength of sensory-motor transmission for visually guided movements. J Neurosci 32:9745–9754. CrossRef Medline
46. Oram MW, Földiák P, Perrett DI, Sengpiel F (1998) The ‘ideal homunculus’: decoding neural population signals. Trends Neurosci 21:259-265. CrossRef Medline
47. Orbán GA, de Wolf J, Maes H (1984) Factors influencing velocity coding in the human visual system. Vision Res 24:33–39. CrossRef Medline
48. Osborne LC (2011) Computation and physiology of sensory-motor processing in eye movements. Curr Opin Neurobiol 21:623-628. CrossRef Medline
49. Osborne LC, Lisberger SG (2009) Spatial and temporal integration of visual motion signals for smooth pursuit eye movements in monkeys. J Neurophysiol 102:2013–2025. CrossRef Medline
50. 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
51. Osborne LC, Lisberger SG, Bialek W (2005) A sensory source for motor variation. Nature 437:412-416. CrossRef Medline
52. Osborne LC, Hohl SS, Bialek W, Lisberger SG (2007) Time course of precision in smooth-pursuit eye movements of monkeys. J Neurosci 27:2987-2998. CrossRef Medline
53. Priebe NJ, Cassanello CR, Lisberger SG (2003) The neural representation of speed in macaque area MT/V5. J Neurosci 23:5650-5661. Medline
54. Rasche C, Gegenfurtner KR (2009) Precision of speed discrimination and smooth pursuit eye movements. Vision Res 49:514-523. CrossRef Medline
55. Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol 159:326-338. CrossRef Medline
56. Salinas E, Abbott LF (1995) Transfer of coded information from sensory to motor Networks. J Neurosci 15:6461-6474. Medline
57. Schrater PR, Knill DC, Simoncelli EP (2000) Mechanism of visual motion detection. Nat Neurosci 3:64–68. CrossRef Medline
58. Schütz AC, Braun DI, Gegenfurtner KR (2011) Eye movements and perception: a selective review. J Vis 11:pi:9. CrossRef Medline
59. Seung HS, Sompolinsky H (1993) Simple models for reading neuronal population codes. Proc Natl Acad Sci U S A 90:10749-10753. CrossRef Medline
60. Shadlen MN, Britten KH, Newsome WT, Movshon JA (1996) A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J Neurosci 16:1486-1510. Medline
61. Simoncini C, Perrinet LU, Montagnini A, Mamassian P, Masson GS (2012) More is not always better: adaptive gain control explains dissociation between perception and action. Nat Neurosci 15:1596-1603. CrossRef Medline
62. Spering M, Montagnini A (2011) Do we track what we see? Common versus independent processing for motion perception and smooth pursuit eye movements: a review. Vision Res 51:836–852. CrossRef Medline
63. Stephens GJ, Osborne LC, Bialek W (2011) Searching for simplicity in the analysis of neurons and behavior. Proc Natl Acad Sci U S A 108:15565-15571. CrossRef Medline
64. Stone LS, Krauzlis RJ (2003) Shared motion signals for human perceptual decisions and oculomotor actions. J Vis 3:725–736. Medline
65. Sun D, Roth S, Black M (2010) Secrets of optical flow estimation and their principles. In: Procedures of IEEE Conference, CVPR, pp 2432–2439. San Francisco, CA.
66. Tychsen L, Lisberger SG (1986) Visual motion processing for the initiation of smooth-pursuit eye movements in humans. J Neurophysiol 56:953-968. Medline
67. van Beers RJ (2007) The sources of variability in saccadic eye movements. J Neurosci 27:8757-8770. CrossRef Medline
68. Watamaniuk SN, Duchon A (1992) The human visual system averages speed information. Vision Res 32:931–941. CrossRef Medline
69. Watamaniuk SN, Heinen SJ (1999) Human smooth pursuit direction discrimination. Vision Res 39:59-70. CrossRef Medline
70. Watamaniuk SN, Sekuler R, Williams DW (1989) Direction perception in complex dynamic displays: the integration of direction information. Vision Res 29:47–59. CrossRef Medline
71. Webb BS, Ledgeway T, Rocchi F (2011) Neural computations governing spatiotemporal pooling of visual motion signals in humans. J Neurosci 31:4917-4925. CrossRef Medline
72. Westwood DA, Goodale MA (2011) Converging evidence for diverging pathways: neuropsychology and psychophysics tell the same story. Vision Res 51:804–811. CrossRef Medline
73. Williams DW, Sekuler R (1984) Coherent global motion percepts from stochastic local motions. Vision Res 24:55-62. CrossRef Medline
74. Williams ZM, Elfar JC, Eskandar EN, Toth LJ, Assad JA (2003) Parietal activity and the perceived direction of ambiguous apparent motion. Nat Neurosci 6:616–623. CrossRef Medline
75. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140-143. CrossRef Medline