Gamma synchrony predicts neuron-neuron correlations and correlations with motor behavior in extrastriate visual area MT

Journal of Neuroscience

Volumn 33, Issue 50, 2013, Pages 19677-19688

  Lee, Joonyeol ^a   Lisberger, Stephen G ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION CORTEX; CONTROLLED STUDY; ELECTRIC POTENTIAL; EVOKED RESPONSE; EXTRASTRIATE BODY AREA; EYE POSITION; GAMMA RHYTHM; LOCOMOTION; MALE; MOVEMENT PERCEPTION; NERVE CELL; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NERVE POTENTIAL; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; RHESUS MONKEY; SMOOTH PURSUIT EYE MOVEMENT; SPIKE WAVE; TASK PERFORMANCE; VISUAL STIMULATION;

ANIMALS; BRAIN MAPPING; MACACA MULATTA; MALE; MOTION PERCEPTION; MOTOR ACTIVITY; NEURONS; PURSUIT, SMOOTH; REACTION TIME; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84889781963     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3478-13.2013     Document Type: Article

References (54)

1. Bair W, Koch C (1996) Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput 8:1185-1202. CrossRef Medline
2. Bair W, O'Keefe LP (1998) The influence of fixational eye movements on the response of neurons in areaMTof the macaque. Vis Neurosci 15:779-786. Medline
3. Berens P, Logothetis NK, Tolias AS (2012) Local field potentials, BOLD and spiking activity: relationships and physiological mechanisms. In: Visual population codes-towards a common multivariate framework for cell recording and functional imaging (Kriegeskorte N, Kreiman G, eds), pp 599-624. Cambridge, MA: MIT.
4. Bokil H, Purpura K, Schoffelen JM, Thomson D, Mitra P (2007) Comparing spectra and coherences for groups of unequal size. J Neurosci Methods 159:337-345. CrossRef Medline
5. Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP (2010) Chronux: a platform for analyzing neural signals. J Neurosci Methods 192:146-151. CrossRef Medline
6. Bosking WH, Maunsell JH (2011) Effects of stimulus direction on the correlation between behavior and single units in area MT during a motion detection task. J Neurosci 31:8230-8238. CrossRef Medline
7. Bosman CA, Schoffelen JM, Brunet N, Oostenveld R, Bastos AM, Womelsdorf T, Rubehn B, Stieglitz T, De Weerd P, Fries P (2012) Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75:875-888. CrossRef Medline
8. 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
9. Buffalo EA, Fries P, Landman R, Buschman TJ, Desimone R (2011) Laminar differences in gamma and alpha coherence in the ventral stream. Proc Natl Acad Sci U S A 108:11262-11267. CrossRef Medline
10. Buracas GT, Zador AM, DeWeese MR, Albright TD (1998) Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20:959-969. CrossRef Medline
11. Cohen MR, Newsome WT (2008) Context-dependent changes in functional circuitry in visual area MT. Neuron 60:162-173. CrossRef Medline
12. Donner TH, Siegel M, Fries P, Engel AK (2009) Buildup of choicepredictive activity in human motor cortex during perceptual decision making. Curr Biol 19:1581-1585. CrossRef Medline
13. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560-1563. CrossRef Medline
14. Gieselmann MA, Thiele A (2008) Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1. Eur J Neurosci 28:447-459. CrossRef Medline
15. Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324:1207-1210. CrossRef Medline
16. Haefner RM, Gerwinn S, Macke JH, Bethge M (2013) Inferring decoding strategies from choice probabilities in the presence of correlated variability. Nat Neurosci 16:235-242. CrossRef Medline
17. Hansen BJ, Chelaru MI, Dragoi V (2012) Correlated variability in laminar cortical circuits. Neuron 76:590-602. CrossRef Medline
18. Henrie JA, Shapley R (2005) LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J Neurophysiol 94:479-490. CrossRef Medline
19. Hohl SS, Lisberger SG (2011) Representation of perceptually invisible image motion in extrastriate visual area MT of macaque monkeys. J Neurosci 31:16561-16569. CrossRef Medline
20. Hohl SS, Chaisanguanthum KS, Lisberger SG (2013) Sensory population decoding for visually guided movements. Neuron 79:167-179. CrossRef Medline
21. 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
22. Jarvis MR, Mitra PP (2001) Sampling properties of the spectrum and coherency of sequences of action potentials. Neural Comput 13:717-749. CrossRef Medline
23. Jia X, Smith MA, Kohn A (2011) Stimulus selectivity and spatial coherence of gamma components of the local field potential. J Neurosci 31:9390-9403. CrossRef Medline
24. Jia X, Tanabe S, Kohn A (2013) Gamma and the coordination of spiking activity in early visual cortex. Neuron 77:762-774. CrossRef Medline
25. Jutras MJ, Fries P, Buffalo EA (2009) Gamma-band synchronization in the macaque hippocampus and memory formation. J Neurosci 29:12521-12531. CrossRef Medline
26. Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach DL, CarandiniM (2009) Local origin of field potentials in visual cortex. Neuron 61:35-41. CrossRef Medline
27. Krauzlis RJ (2003) Neuronal activity in the rostral superior colliculus related to the initiation of pursuit and saccadic eye movements. J Neurosci 23:4333-4344. Medline
28. Le Digabel S (2011) Algorithm 909: NOMAD: nonlinear optimization with the MADS algorithm. ACM Trans Math Softw 37:1-15. CrossRef
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. Liu J, Newsome WT (2003) Functional organization of speed tuned neurons in visual area MT. J Neurophysiol 89:246-256. Medline
31. Liu J, Newsome WT (2006) Local field potential in cortical area MT: stimulus tuning and behavioral correlations. J Neurosci 26:7779-7790. CrossRef Medline
32. 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
33. Mitra PP, Pesaran B (1999) Analysis of dynamic brain imaging data. Biophys J 76:691-708. CrossRef Medline
34. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37-100. Medline
35. Morris EJ, Lisberger SG (1987) Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. J Neurophysiol 58:1351-1369. Medline
36. Nienborg H, Cumming BG (2006) Macaque V2 neurons, but not V1 neurons, show choice-related activity. J Neurosci 26:9567-9578. CrossRef Medline
37. Nienborg H, Cumming B (2010) 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. CrossRef Medline
38. 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
39. Osborne LC, Lisberger SG, Bialek W (2005) A sensory source for motor variation. Nature 437:412-416. CrossRef Medline
40. Palmer C, Cheng SY, Seidemann E (2007) Linking neuronal and behavioral performance in a reaction-time visual detection task. J Neurosci 27:8122-8137. CrossRef Medline
41. Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (2002) Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5:805-811. CrossRef Medline
42. Ramachandran R, Lisberger SG (2005) Normal performance and expression of learning in the vestibulo-ocular reflex (VOR) at high frequencies. J Neurophysiol 93:2028-2038. Medline
43. Ray S, Maunsell JH (2010) Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 67:885-896. CrossRef Medline
44. Ray S, Maunsell JH (2011) Different origins of gamma rhythm and highgamma activity in macaque visual cortex. PLoS Biol 9:e1000610. CrossRef Medline
45. Ray S, Ni AM, Maunsell JH (2013) Strength of gamma rhythm depends on normalization. PLoS Biol 11:e1001477. CrossRef Medline
46. Roberts MJ, Lowet E, Brunet NM, Ter Wal M, Tiesinga P, Fries P, De Weerd P (2013) Robust gamma coherence between macaque V1 and V2 by dynamic frequency matching. Neuron 78:523-536. CrossRef Medline
47. Schoffelen JM, Oostenveld R, Fries P (2005) Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308:111-113. CrossRef Medline
48. Schoppik D, Nagel KI, Lisberger SG (2008) Cortical mechanisms of smooth eye movements revealed by dynamic covariations of neural and behavioral responses. Neuron 58:248-260. CrossRef Medline
49. 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
50. Smith MA, Jia X, Zandvakili A, Kohn A (2013) Laminar dependence of neuronal correlations in visual cortex. J Neurophysiol 109:940-947. CrossRef Medline
51. Snyder LH, Dickinson AR, Calton JL (2006) Preparatory delay activity in the monkey parietal reach region predicts reach reaction times. J Neurosci 26:10091-10099. CrossRef Medline
52. Womelsdorf T, Fries P, Mitra PP, Desimone R (2006) Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439:733-736. CrossRef Medline
53. Womelsdorf T, Lima B, Vinck M, Oostenveld R, Singer W, Neuenschwander S, Fries P (2012) Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle. Proc Natl Acad Sci U S A 109:4302-4307. CrossRef Medline
54. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140-143. CrossRef Medline