A Map of Anticipatory Activity in Mouse Motor Cortex

Neuron

Volumn 94, Issue 4, 2017, Pages 866-879.e4

  Chen, Tsai Wen ^a,b   Li, Nuo ^a   Daie, Kayvon ^a   Svoboda, Karel ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

calcium; decision; gcamp; gcamp6; motor cortex; motor planning; persistent activity; short term memory; two photon

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR LATERAL MOTOR CORTEX; ANTICIPATORY ACTIVITY; ARTICLE; BRAIN MAPPING; BRAIN NERVE CELL; CODING; CONTROLLED STUDY; FRONTAL CORTEX; MALE; MOTOR ACTIVITY; MOTOR CORTEX; MOUSE; NEUROIMAGING; NONHUMAN; PREDICTION; PRIORITY JOURNAL; TACTILE STIMULATION; TASK PERFORMANCE; ANIMAL; AXON; DECISION MAKING; FLUORESCENCE IMAGING; IMAGE PROCESSING; METABOLISM; NERVE CELL; PHYSIOLOGY; PYRAMIDAL TRACT; TOUCH; VIBRISSA;

CALCIUM;

ANIMALS; AXONS; BEHAVIOR, ANIMAL; CALCIUM; DECISION MAKING; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MOTOR ACTIVITY; MOTOR CORTEX; NEURONS; OPTICAL IMAGING; PYRAMIDAL TRACTS; TOUCH; VIBRISSAE;

EID: 85020102362     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2017.05.005     Document Type: Article

References (77)

1. Akerboom, J., Chen, T.W., Wardill, T.J., Tian, L., Marvin, J.S., Mutlu, S., Calderón, N.C., Esposti, F., Borghuis, B.G., Sun, X.R., et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32 (2012), 13819–13840.
2. Amador, N., Schlag-Rey, M., Schlag, J., Reward-predicting and reward-detecting neuronal activity in the primate supplementary eye field. J. Neurophysiol. 84 (2000), 2166–2170.
3. Amiez, C., Joseph, J.P., Procyk, E., Reward encoding in the monkey anterior cingulate cortex. Cereb. Cortex 16 (2006), 1040–1055.
4. Brecht, M., Movement, confusion, and orienting in frontal cortices. Neuron 72 (2011), 193–196.
5. Brown, S.P., Hestrin, S., Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457 (2009), 1133–1136.
6. Bruce, C.J., Goldberg, M.E., Primate frontal eye fields. I. Single neurons discharging before saccades. J. Neurophysiol. 53 (1985), 603–635.
7. Chakrabarti, S., Zhang, M., Alloway, K.D., MI neuronal responses to peripheral whisker stimulation: relationship to neuronal activity in si barrels and septa. J. Neurophysiol. 100 (2008), 50–63.
8. Chen, T.-W. (2008). A Systems level analysis of neuronal network function in the olfactory bulb: coding, connectivity, and modular organization. PhD Thesis (University of Göttingen).
9. Chen, T.W., Wardill, T.J., Sun, Y., Pulver, S.R., Renninger, S.L., Baohan, A., Schreiter, E.R., Kerr, R.A., Orger, M.B., Jayaraman, V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499 (2013), 295–300.
10. Churchland, M.M., Shenoy, K.V., Delay of movement caused by disruption of cortical preparatory activity. J. Neurophysiol. 97 (2007), 348–359.
11. Churchland, M.M., Cunningham, J.P., Kaufman, M.T., Ryu, S.I., Shenoy, K.V., Cortical preparatory activity: representation of movement or first cog in a dynamical machine?. Neuron 68 (2010), 387–400.
12. Crutcher, M.D., Alexander, G.E., Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey. J. Neurophysiol. 64 (1990), 151–163.
13. Dana, H., Chen, T.-W., Hu, A., Shields, B.C., Guo, C., Looger, L.L., Kim, D.S., Svoboda, K., Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS ONE, 9, 2014, e108697.
14. Dana, H., Mohar, B., Sun, Y., Narayan, S., Gordus, A., Hasseman, J.P., Tsegaye, G., Holt, G.T., Hu, A., Walpita, D., et al. Sensitive red protein calcium indicators for imaging neural activity. eLife, 5, 2016, 5.
15. Ding, L., Gold, J.I., Caudate encodes multiple computations for perceptual decisions. J. Neurosci. 30 (2010), 15747–15759.
16. Erlich, J.C., Bialek, M., Brody, C.D., A cortical substrate for memory-guided orienting in the rat. Neuron 72 (2011), 330–343.
17. Erlich, J.C., Brunton, B.W., Duan, C.A., Hanks, T.D., Brody, C.D., Distinct effects of prefrontal and parietal cortex inactivations on an accumulation of evidence task in the rat. eLife, 4, 2015, 4.
18. Ferezou, I., Haiss, F., Gentet, L.J., Aronoff, R., Weber, B., Petersen, C.C., Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56 (2007), 907–923.
19. Fried, I., Mukamel, R., Kreiman, G., Internally generated preactivation of single neurons in human medial frontal cortex predicts volition. Neuron 69 (2011), 548–562.
20. Funahashi, S., Bruce, C.J., Goldman-Rakic, P.S., Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61 (1989), 331–349.
21. Goard, M.J., Pho, G.N., Woodson, J., Sur, M., Distinct roles of visual, parietal, and frontal motor cortices in memory-guided sensorimotor decisions. eLife, 5, 2016, 5.
22. Guo, Z.V., Hires, S.A., Li, N., O'Connor, D.H., Komiyama, T., Ophir, E., Huber, D., Bonardi, C., Morandell, K., Gutnisky, D., et al. Procedures for behavioral experiments in head-fixed mice. PLoS ONE, 9, 2014, e88678.
23. Guo, Z.V., Li, N., Huber, D., Ophir, E., Gutnisky, D., Ting, J.T., Feng, G., Svoboda, K., Flow of cortical activity underlying a tactile decision in mice. Neuron 81 (2014), 179–194.
24. Guo, Z.V., Inagaki, H., Daie, K., Druckmann, S., Gerfen, C.R., Svoboda, K., Maintenance of persistent activity in a frontal thalamocortical loop. Nature, 2017, 10.1038/nature22324 Published online May 3, 2017.
25. Hernández, A., Nácher, V., Luna, R., Zainos, A., Lemus, L., Alvarez, M., Vázquez, Y., Camarillo, L., Romo, R., Decoding a perceptual decision process across cortex. Neuron 66 (2010), 300–314.
26. Hill, D.N., Curtis, J.C., Moore, J.D., Kleinfeld, D., Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 72 (2011), 344–356.
27. Hooks, B.M., Hires, S.A., Zhang, Y.X., Huber, D., Petreanu, L., Svoboda, K., Shepherd, G.M., Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol., 9, 2011, e1000572.
28. Hooks, B.M., Mao, T., Gutnisky, D.A., Yamawaki, N., Svoboda, K., Shepherd, G.M., Organization of cortical and thalamic input to pyramidal neurons in mouse motor cortex. J. Neurosci. 33 (2013), 748–760.
29. Howe, M.W., Tierney, P.L., Sandberg, S.G., Phillips, P.E., Graybiel, A.M., Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 500 (2013), 575–579.
30. Huber, D., Gutnisky, D.A., Peron, S., O'Connor, D.H., Wiegert, J.S., Tian, L., Oertner, T.G., Looger, L.L., Svoboda, K., Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484 (2012), 473–478.
31. Junek, S., Chen, T.W., Alevra, M., Schild, D., Activity correlation imaging: visualizing function and structure of neuronal populations. Biophys. J. 96 (2009), 3801–3809.
32. Kerkhoff, G., Spatial hemineglect in humans. Prog. Neurobiol. 63 (2001), 1–27.
33. Kerlin, A.M., Andermann, M.L., Berezovskii, V.K., Reid, R.C., Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67 (2010), 858–871.
34. Kiritani, T., Wickersham, I.R., Seung, H.S., Shepherd, G.M., Hierarchical connectivity and connection-specific dynamics in the corticospinal-corticostriatal microcircuit in mouse motor cortex. J. Neurosci. 32 (2012), 4992–5001.
35. Kleinfeld, D., Sachdev, R.N., Merchant, L.M., Jarvis, M.R., Ebner, F.F., Adaptive filtering of vibrissa input in motor cortex of rat. Neuron 34 (2002), 1021–1034.
36. Komiyama, T., Sato, T.R., O'Connor, D.H., Zhang, Y.X., Huber, D., Hooks, B.M., Gabitto, M., Svoboda, K., Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464 (2010), 1182–1186.
37. Krupa, D.J., Ghazanfar, A.A., Nicolelis, M.A., Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc. Natl. Acad. Sci. USA 96 (1999), 8200–8205.
38. Li, N., Chen, T.W., Guo, Z.V., Gerfen, C.R., Svoboda, K., A motor cortex circuit for motor planning and movement. Nature 519 (2015), 51–56.
39. Li, N., Daie, K., Svoboda, K., Druckmann, S., Robust neuronal dynamics in premotor cortex during motor planning. Nature 532 (2016), 459–464.
40. Lin, B.J., Chen, T.W., Schild, D., Cell type-specific relationships between spiking and [Ca2+]i in neurons of the Xenopus tadpole olfactory bulb. J. Physiol. 582 (2007), 163–175.
41. Lur, G., Vinck, M.A., Tang, L., Cardin, J.A., Higley, M.J., Projection-Specific Visual Feature Encoding by Layer 5 Cortical Subnetworks. Cell Rep. 14 (2016), 2538–2545.
42. Madisen, L., Garner, A.R., Shimaoka, D., Chuong, A.S., Klapoetke, N.C., Li, L., van der Bourg, A., Niino, Y., Egolf, L., Monetti, C., et al. Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85 (2015), 942–958.
43. Maimon, G., Assad, J.A., A cognitive signal for the proactive timing of action in macaque LIP. Nat. Neurosci. 9 (2006), 948–955.
44. Mao, T., Kusefoglu, D., Hooks, B.M., Huber, D., Petreanu, L., Svoboda, K., Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72 (2011), 111–123.
45. Matsumoto, M., Matsumoto, K., Abe, H., Tanaka, K., Medial prefrontal cell activity signaling prediction errors of action values. Nat. Neurosci. 10 (2007), 647–656.
46. Matyas, F., Sreenivasan, V., Marbach, F., Wacongne, C., Barsy, B., Mateo, C., Aronoff, R., Petersen, C.C., Motor control by sensory cortex. Science 330 (2010), 1240–1243.
47. Morishima, M., Kawaguchi, Y., Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci. 26 (2006), 4394–4405.
48. Neafsey, E.J., Bold, E.L., Haas, G., Hurley-Gius, K.M., Quirk, G., Sievert, C.F., Terreberry, R.R., The organization of the rat motor cortex: a microstimulation mapping study. Brain Res. 396 (1986), 77–96.
49. Ohmae, S., Uematsu, A., Tanaka, M., Temporally specific sensory signals for the detection of stimulus omission in the primate deep cerebellar nuclei. J. Neurosci. 33 (2013), 15432–15441.
50. Peron, S., Chen, T.W., Svoboda, K., Comprehensive imaging of cortical networks. Curr. Opin. Neurobiol. 32 (2015), 115–123.
51. Petreanu, L., Mao, T., Sternson, S.M., Svoboda, K., The subcellular organization of neocortical excitatory connections. Nature 457 (2009), 1142–1145.
52. Petreanu, L., Gutnisky, D.A., Huber, D., Xu, N.L., O'Connor, D.H., Tian, L., Looger, L., Svoboda, K., Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489 (2012), 299–303.
53. Pnevmatikakis, E.A., Soudry, D., Gao, Y., Machado, T.A., Merel, J., Pfau, D., Reardon, T., Mu, Y., Lacefield, C., Yang, W., et al. Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89 (2016), 285–299.
54. Pologruto, T.A., Sabatini, B.L., Svoboda, K., ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online, 2, 2003, 13.
55. Riehle, A., Requin, J., Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. J. Neurophysiol. 61 (1989), 534–549.
56. Rigotti, M., Barak, O., Warden, M.R., Wang, X.J., Daw, N.D., Miller, E.K., Fusi, S., The importance of mixed selectivity in complex cognitive tasks. Nature 497 (2013), 585–590.
57. Rizzolatti, G., Matelli, M., Pavesi, G., Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106 (1983), 655–673.
58. Rossi, M.A., Li, H.E., Lu, D., Kim, I.H., Bartholomew, R.A., Gaidis, E., Barter, J.W., Kim, N., Cai, M.T., Soderling, S.H., Yin, H.H., A GABAergic nigrotectal pathway for coordination of drinking behavior. Nat. Neurosci. 19 (2016), 742–748.
59. Schall, J.D., Thompson, K.G., Neural selection and control of visually guided eye movements. Annu. Rev. Neurosci. 22 (1999), 241–259.
60. Scott, S.H., Inconvenient truths about neural processing in primary motor cortex. J. Physiol. 586 (2008), 1217–1224.
61. Shenoy, K.V., Sahani, M., Churchland, M.M., Cortical control of arm movements: a dynamical systems perspective. Annu. Rev. Neurosci. 36 (2013), 337–359.
62. Shepherd, G.M., Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14 (2013), 278–291.
63. Sofroniew, N.J., Flickinger, D., King, J., Svoboda, K., A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging. eLife, 5, 2016, 5.
64. Sommer, M.A., Wurtz, R.H., Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J. Neurophysiol. 83 (2000), 1979–2001.
65. Stanek, E. 4th, Cheng, S., Takatoh, J., Han, B.X., Wang, F., Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination. eLife, 3, 2014, e02511.
66. Stuphorn, V., Taylor, T.L., Schall, J.D., Performance monitoring by the supplementary eye field. Nature 408 (2000), 857–860.
67. Sul, J.H., Jo, S., Lee, D., Jung, M.W., Role of rodent secondary motor cortex in value-based action selection. Nat. Neurosci. 14 (2011), 1202–1208.
68. Tanaka, M., Cognitive signals in the primate motor thalamus predict saccade timing. J. Neurosci. 27 (2007), 12109–12118.
69. Tanji, J., Evarts, E.V., Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J. Neurophysiol. 39 (1976), 1062–1068.
70. Tennant, K.A., Adkins, D.L., Donlan, N.A., Asay, A.L., Thomas, N., Kleim, J.A., Jones, T.A., The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb. Cortex 21 (2011), 865–876.
71. Theis, L., Berens, P., Froudarakis, E., Reimer, J., Román Rosón, M., Baden, T., Euler, T., Tolias, A.S., Bethge, M., Benchmarking spike rate inference in population calcium imaging. Neuron 90 (2016), 471–482.
72. Thévenaz, P., Ruttimann, U.E., Unser, M., A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7 (1998), 27–41.
73. Trachtenberg, J.T., Chen, B.E., Knott, G.W., Feng, G., Sanes, J.R., Welker, E., Svoboda, K., Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420 (2002), 788–794.
74. Travers, J.B., Dinardo, L.A., Karimnamazi, H., Motor and premotor mechanisms of licking. Neurosci. Biobehav. Rev. 21 (1997), 631–647.
75. Turner, R.S., DeLong, M.R., Corticostriatal activity in primary motor cortex of the macaque. J. Neurosci. 20 (2000), 7096–7108.
76. Vanni, M.P., Murphy, T.H., Mesoscale transcranial spontaneous activity mapping in GCaMP3 transgenic mice reveals extensive reciprocal connections between areas of somatomotor cortex. J. Neurosci. 34 (2014), 15931–15946.
77. Vogelstein, J.T., Watson, B.O., Packer, A.M., Yuste, R., Jedynak, B., Paninski, L., Spike inference from calcium imaging using sequential Monte Carlo methods. Biophys. J. 97 (2009), 636–655.