V1 neurons respond differently to object motion versus motion from eye movements

Nature Communications

Volumn 6, Issue , 2015, Pages

  Troncoso, Xoana G ^a,b   McCamy, Michael B ^a   Jazi, Ali Najafian ^a,c   Cui, Jie ^a   Otero Millan, Jorge ^a,d   MacKnik, Stephen L ^a,e   Costela, Francisco M ^a,c   Martinez Conde, Susana ^a,e  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

^b Unite de Neurosciences Integratives et Computationnelles   (France)

^c ARIZONA STATE UNIVERSITY   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; EYE; NEUROLOGY; PROTEIN; VISION;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXTRAOCULAR MUSCLE; EYE FIXATION; EYE MOVEMENT; FIRING RATE; INFORMATION PROCESSING; NERVE CELL; NERVE POTENTIAL; NONHUMAN; RECEPTIVE FIELD; RHESUS MONKEY; SACCADIC EYE MOVEMENT; SACCADIC SUPPRESSION; STRIATE CORTEX; VISUAL MASKING; VISUAL STIMULATION;

PRIMATES;

EID: 84941695305     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9114     Document Type: Article

References (56)

1. Cullen, K. E. Sensory signals during active versus passive movement. Curr. Opin. Neurobiol. 14, 698-706 (2004).
2. Crapse, T. B., Sommer, M. A. Corollary discharge across the animal kingdom. Nat. Rev. Neurosci. 9, 587-600 (2008).
3. Sommer, M. A., Wurtz, R. H. Brain circuits for the internal monitoring of movements. Annu. Rev. Neurosci. 31, 317-338 (2008).
4. Crapse, T. B., Sommer, M. A. Corollary discharge circuits in the primate brain. Curr. Opin. Neurobiol. 18, 552-557 (2008).
5. Wurtz, R. H. Visual cortex neurons: response to stimuli during rapid eye movements. Science 162, 1148-1150 (1968).
6. Wurtz, R. H. Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J. Neurophysiol. 32, 987-994 (1969).
7. Wurtz, R. H. Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. J. Neurophysiol. 32, 975-986 (1969).
8. Battaglini, P. P., Galletti, C., Aicardi, G., Squatrito, S., Maioli, M. G. Effect of fast moving stimuli and saccadic eye movements on cell activity in visual areas V1 and V2 of behaving monkeys. Arch. Ital. Biol. 124, 111-119 (1986).
9. Bridgeman, B. Visual receptive fields sensitive to absolute and relative motion during tracking. Science 178, 1106-1108 (1972).
10. Fischer, B., Boch, R., Bach, M. Stimulus versus eye movements: comparison of neural activity in the striate and prelunate visual cortex (A17 and A19) of trained rhesus monkey. Exp. Brain Res. 43, 69-77 (1981).
11. Galletti, C., Squatrito, S., Paolo Battaglini, P., Maioli, M. G. 'Real-motion' cells in the primary visual cortex of macaque monkeys. Brain Res. 301, 95-110 (1984).
12. IIg, U. J., Thier, P. Inability of rhesus monkey area V1 to discriminate between self-induced and externally induced retinal image slip. Eur. J. Neurosci. 8, 1156-1166 (1996).
13. Wurtz, R. H. Neuronal mechanisms of visual stability. Vision Res. 48, 2070-2089 (2008).
14. Goldberg, M. E., Wurtz, R. H. Activity of superior colliculus in behaving monkey-ll. Effect of attention on neuronal responses. J. Neurophysiol. 35, 560-574 (1972).
15. Chen, Y. et al. Task difficulty modulates the activity of specific neuronal populations in primary visual cortex. Nat. Neurosci. 11, 974-982 (2008).
16. Briggs, F., Mangun, G. R., Usrey, W. M. Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits. Nature 499, 476-480 (2013).
17. Martinez-Conde, S., Macknik, S. L., Hubel, D. H. The role of fixational eye movements in visual perception. Nat. Rev. Neurosci. 5, 229-240 (2004).
18. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., Hubel, D. H. Microsaccades: a neurophysiological analysis. Trends Neurosci. 32, 463-475 (2009).
19. Martinez-Conde, S., Otero-Millan, J., Macknik, S. L. The impact of microsaccades on vision: towards a unified theory of saccadic function. Nat. Rev. Neurosci. 14, 83-96 (2013).
20. Ross, J., Morrone, M. C., Goldberg, M., Burr, D. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113-121 (2001).
21. Beeler, G. W. Visual threshold changes resulting from spontaneous saccadic eye movements. Vision Res. 7, 769-775 (1967).
22. Zuber, B. L., Stark, L. Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. Exp. Neurol. 16, 65-79 (1966).
23. Ditchburn, R. W. Eye-movements in relation to retinal action. Opt. Acta 1, 171-176 (1955).
24. Krauskopf, J., Graf, V., Gaarder, K. Lack of inhibition during involuntary saccades. Am. J. Psychol. 79, 73-81 (1966).
25. Sperling, G. in Eye Movements and their Role in Visual and Cognitive Processes (ed. Kowler, E.) 307-351 (Elsevier Biomedical Press, 1990).
26. Macknik, S. L., Fisher, B. D., Bridgeman, B. Flicker distorts visual space constancy. Vis. Res. 31, 2057-2064 (1991).
27. Bridgeman, B., Macknik, S. L. Saccadic suppression relies on luminance information. Psychol. Res. 58, 163-168 (1995).
28. Burr, D. Eye Movements: keeping vision stable. Curr. Biol. 14, R195-R197 (2004).
29. Carandini, M., Heeger, D. J., Movshon, J. A. in Models of Cortical Circuits 401-443 (Springer, 1999).
30. Schwartz, O., Chichilnisky, E. J., Simoncelli, E. P. Characterizing neural gain control using spike-triggered covariance. Adv. Neural Inform. Process. Syst. 14, 269-276 (2002).
31. Kim, H. R., Angelaki, D. E., DeAngelis, G. C. A functional link between MT neurons and depth perception based on motion parallax. J. Neurosci. 35, 2766-2777 (2015).
32. Lappe, M., Bremmer, F., Van den Berg, A. V. Perception of self-motion from visual flow. Trends Cogn. Sci. 3, 329-336 (1999).
33. Gibson, J. J. The perception of the visual world. Available at ohttp://psycnet.apa.org/psycinfo/1951-04286-0004 (1950).
34. Trotter, Y., Celebrini, S., Beaux, J. C., Grandjean, B. Neuronal stereoscopic processing following extraocular proprioception deafferentation. Neuroreport 1, 187-190 (1990).
35. Wang, X., Zhang, M., Cohen, I. S., Goldberg, M. E. The proprioceptive representation of eye position in monkey primary somatosensory cortex. Nat. Neurosci. 10, 640-646 (2007).
36. Berman, R. A., Wurtz, R. H. Functional identification of a pulvinar path from superior colliculus to cortical area MT. J. Neurosci. 30, 6342-6354 (2010).
37. Wurtz, R. H., McAlonan, K., Cavanaugh, J., Berman, R. A. Thalamic pathways for active vision. Trends Cogn. Sci. 15, 177-184 (2011).
38. Berman, R. A., Wurtz, R. H. Signals conveyed in the pulvinar pathway from superior colliculus to cortical area MT. J. Neurosci. 31, 373-384 (2011).
39. Hafed, Z. M. Alteration of visual perception prior to microsaccades. Neuron 77, 775-786 (2013).
40. Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron 21, 761-773 (1998).
41. McAdams, C. J., Reid, R. C. Attention modulates the responses of simple cells in monkey primary visual cortex. J. Neurosci. 25, 11023-11033 (2005).
42. Xing, D., Ringach, D. L., Hawken, M. J., Shapley, R. M. Untuned suppression makes a major contribution to the enhancement of orientation selectivity in macaque V1. J. Neurosci. 31, 15972-15982 (2011).
43. Schroeder, C. E., Wilson, D. A., Radman, T., Scharfman, H., Lakatos, P. Dynamics of active sensing and perceptual selection. Curr. Opin. Neurobiol. 20, 172-176 (2010).
44. Baudot, P. et al. Animation of natural scene by virtual eye-movements evokes high precision and low noise in V1 neurons. Front. Neural Circuits 7, 206 (2013).
45. Romo, R., Hernández, A., Zainos, A., Brody, C., Salinas, E. Exploring the cortical evidence of a sensory-discrimination process. Philos. Trans. R Soc. Lond. B 357, 1039-1051 (2002).
46. Martinez-Conde, S., Macknik, S. L., Hubel, D. H. Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nat. Neurosci. 3, 251-258 (2000).
47. Thiele, A., Henning, P., Kubischik, M., Hoffmann, K.-P. Neural mechanisms of saccadic suppression. Science 295, 2460-2462 (2002).
48. Engbert, R., Mergenthaler, K. Microsaccades are triggered by low retinal image slip. Proc. Natl Acad. Sci. USA 103, 7192-7197 (2006).
49. Engbert, R., Kliegl, R. Microsaccades uncover the orientation of covert attention. Vision Res. 43, 1035-1045 (2003).
50. Engbert, R. Microsaccades: a microcosm for research on oculomotor control, attention, and visual perception. Prog. Brain Res. 154, 177-192 (2006).
51. Laubrock, J., Engbert, R., Kliegl, R. Microsaccade dynamics during covert attention. Vision Res. 45, 721-730 (2005).
52. Møller, F., Laursen, M., Tygesen, J., Sjølie, A. Binocular quantification and characterization of microsaccades. Graefes Arch. Clin. Exp. Ophthalmol. 240, 765-770 (2002).
53. Betta, E., Turatto, M. Are you ready? I can tell by looking at your microsaccades. Neuroreport 17, 1001 (2006).
54. McCamy, M. B. et al. Simultaneous recordings of ocular microtremor and microsaccades with a piezoelectric sensor and a video-oculography system. PeerJ. 1, e14 (2013).
55. McCamy, M. B., Najafian Jazi, A., Otero-Millan, J., Macknik, S. L., Martinez-Conde, S. The effects of fixation target size and luminance on microsaccades and square-wave jerks. PeerJ. 1, e9 (2013).
56. Reppas, J. B., Usrey, W. M., Reid, R. C. Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35, 961-974 (2002).