Reorganization of cortical population activity imaged throughout long-term sensory deprivation

Nature Neuroscience

Volumn 15, Issue 11, 2012, Pages 1539-1546

  Margolis, David J ^a   Lütcke, Henry ^a   Schulz, Kristina ^a   Haiss, Florent ^a   Weber, Bruno ^a   Kügler, Sebastian ^b   Hasan, Mazahir T ^c,d   Helmchen, Fritjof ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; INFORMATION PROCESSING; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SENSORY DEPRIVATION; SENSORY STIMULATION; SOMATOSENSORY CORTEX; VIBRISSA;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; CALCIUM; CEREBRAL CORTEX; COMPUTER SIMULATION; FEMALE; GENE EXPRESSION REGULATION; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; NEURONS; NEUROPIL; OPTICS AND PHOTONICS; PHYSICAL STIMULATION; SENSORY DEPRIVATION; SYNAPSINS; TIME FACTORS; TRANSDUCTION, GENETIC; VIBRISSAE;

EID: 84868210837     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3240     Document Type: Article

References (56)

1. Buonomano, D.V. & Merzenich, M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149-186 (1998). (Pubitemid 28150662)
2. Feldman, D.E. Synaptic mechanisms for plasticity in neocortex. Annu. Rev. Neurosci. 32, 33-55 (2009).
3. Simons, D.J. & Land, P.W. Early experience of tactile stimulation infuences organization of somatic sensory cortex. Nature 326, 694-697 (1987). (Pubitemid 17059787)
4. Petersen, C.C. The functional organization of the barrel cortex. Neuron 56, 339-355 (2007).
5. Feldman, D.E. & Brecht, M. Map plasticity in somatosensory cortex. Science 310, 810-815 (2005). (Pubitemid 41567332)
6. Fox, K. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111, 799-814 (2002). (Pubitemid 34603250)
7. Diamond, M.E., Huang, W. & Ebner, F. F. Laminar comparison of somatosensory cortical plasticity. Science 265, 1885-1888 (1994). (Pubitemid 24324248)
8. Glazewski, S. & Fox, K. Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J. Neurophysiol. 75, 1714-1729 (1996). (Pubitemid 26114075)
9. Cheetham, C.E., Hammond, M.S., Edwards, C.E. & Finnerty, G.T. Sensory experience alters cortical connectivity and synaptic function site specifcally. J. Neurosci. 27, 3456-3465 (2007). (Pubitemid 46515126)
10. Glazewski, S., Chen, C.M., Silva, A. & Fox, K. Requirement for alpha-CaMKII in experience-dependent plasticity of the barrel cortex. Science 272, 421-423 (1996). (Pubitemid 26138181)
11. Oberlaender, M., Ramirez, A. & Bruno, R.M. Sensory experience restructures thalamocortical axons during adulthood. Neuron 74, 648-655 (2012).
12. Brecht, M., Roth, A. & Sakmann, B. Dynamic receptive felds of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J. Physiol. (Lond.) 553, 243-265 (2003). (Pubitemid 37483932)
13. Crochet, S. & Petersen, C.C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 9, 608-610 (2006). (Pubitemid 44012257)
14. Kerr, J.N. et al. Spatial organization of neuronal population responses in layer 2/3 of rat barrel cortex. J. Neurosci. 27, 13316-13328 (2007). (Pubitemid 350220486)
15. Sato, T.R., Gray, N.W., Mainen, Z.F. & Svoboda, K. The functional microarchitecture of the mouse barrel cortex. PLoS Biol. 5, e189 (2007).
16. Rothschild, G., Nelken, I. & Mizrahi, A. Functional organization and population dynamics in the mouse primary auditory cortex. Nat. Neurosci. 13, 353-360 (2010).
17. Polley, D.B., Chen-Bee, C.H. & Frostig, R.D. Two directions of plasticity in the sensory-deprived adult cortex. Neuron 24, 623-637 (1999).
18. Brecht, M., Schneider, M. & Manns, I.D. Silent neurons in sensorimotor cortices: implications for plasticity. in Neural Plasticity in Adult Somatic Sensory-Motor Systems (ed. Ebner, F.F.), 1-19 (CRC Press, 2005).
19. Shoham, S., O'Connor, D.H. & Segev, R. How silent is the brain: is there a "dark matter" problem in neuroscience? J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 192, 777-784 (2006). (Pubitemid 44126180)
20. Jacob, V., Petreanu, L., Wright, N., Svoboda, K. & Fox, K. Regular spiking and intrinsic bursting pyramidal cells show orthogonal forms of experience-dependent plasticity in layer V of barrel cortex. Neuron 73, 391-404 (2012).
21. Andermann, M.L., Kerlin, A.M. & Reid, R.C. Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing. Front Cell Neurosci 4, 3 (2010).
22. Mank, M., et al. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5, 805-811 (2008).
23. Tian, L. et al. Imaging neural activity in worms, fies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881 (2009).
24. Lütcke, H. et al. Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice. Front Neural Circuits 4, 9 (2010).
25. Nagai, T., Yamada, S., Tominaga, T., Ichikawa, M. & Miyawaki, A. Expanded dynamic range of fuorescent indicators for Ca(2+) by circularly permuted yellow fuorescent proteins. Proc. Natl. Acad. Sci. USA 101, 10554-10559 (2004). (Pubitemid 38955780)
26. Holtmaat, A. et al. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144 (2009).
27. Minderer, M. et al. Chronic imaging of cortical sensory map dynamics using a genetically encoded calcium indicator. J. Physiol. (Lond.) 590, 99-107 (2012).
28. Yassin, L. et al. An embedded subnetwork of highly active neurons in the neocortex. Neuron 68, 1043-1050 (2010).
29. Wallace, D.J. et al. Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor. Nat. Methods 5, 797-804 (2008).
30. Clem, R.L., Celikel, T. & Barth, A.L. Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319, 101-104 (2008).
31. Lefort, S., Tomm, C., Floyd Sarria, J.C. & Petersen, C.C. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61, 301-316 (2009).
32. Glazewski, S., Giese, K.P., Silva, A. & Fox, K. The role of alpha-CaMKII autophosphorylation in neocortical experience-dependent plasticity. Nat. Neurosci. 3, 911-918 (2000).
33. Barth, A.L. & Poulet, J.F. Experimental evidence for sparse fring in the neocortex. Trends Neurosci. 35, 345-355 (2012).
34. Crochet, S., Poulet, J.F., Kremer, Y. & Petersen, C.C. Synaptic mechanisms underlying sparse coding of active touch. Neuron 69, 1160-1175 (2011).
35. O'Connor, D.H., Peron, S.P., Huber, D. & Svoboda, K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67, 1048-1061 (2010).
36. Yazaki-Sugiyama, Y., Kang, S., Cateau, H., Fukai, T. & Hensch, T.K. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462, 218-221 (2009).
37. Gandhi, S.P., Yanagawa, Y. & Stryker, M.P. Delayed plasticity of inhibitory neurons in developing visual cortex. Proc. Natl. Acad. Sci. USA 105, 16797-16802 (2008).
38. Hofer, S.B. et al. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat. Neurosci. 14, 1045-1052 (2011).
39. Gentet, L.J. et al. Unique functional properties of somatostatin- expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612 (2012).
40. Nelson, S.B. & Turrigiano, G.G. Strength through diversity. Neuron 60, 477-482 (2008).
41. Turrigiano, G.G. & Nelson, S.B. Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358-364 (2000). (Pubitemid 30389303)
42. Diamond, M.E., Armstrong-James, M. & Ebner, F.F. Experience-dependent plasticity in adult rat barrel cortex. Proc. Natl. Acad. Sci. USA 90, 2082-2086 (1993). (Pubitemid 23070002)
43. Celikel, T., Szostak, V.A. & Feldman, D.E. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat. Neurosci. 7, 534-541 (2004). (Pubitemid 38544593)
44. Hebb, D.O. The Organization of Behavior: A Neuropsychological Theory (Wiley, New York, 1949).
45. Wen, J.A. & Barth, A.L. Input-specifc critical periods for experience-dependent plasticity in layer 2/3 pyramidal neurons. J. Neurosci. 31, 4456-4465 (2011).
46. Mrsic-Flogel, T.D. et al. Homeostatic regulation of eye-specifc responses in visual cortex during ocular dominance plasticity. Neuron 54, 961-972 (2007). (Pubitemid 46907503)
47. Cheetham, C.E., Hammond, M.S., McFarlane, R. & Finnerty, G.T. Altered sensory experience induces targeted rewiring of local excitatory connections in mature neocortex. J. Neurosci. 28, 9249-9260 (2008).
48. Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473-478 (2012).
49. Yamada, Y. et al. Quantitative comparison of genetically encoded Ca indicators in cortical pyramidal cells and cerebellar Purkinje cells. Front Cell Neurosci 5, 18 (2011).
50. Hübener, M. & Bonhoeffer, T. Searching for engrams. Neuron 67, 363-371 (2010).
51. Mastakov, M.Y., Baer, K., Xu, R., Fitzsimons, H. & During, M.J. Combined injection of rAAV with mannitol enhances gene expression in the rat brain. Mol. Ther. 3, 225-232 (2001). (Pubitemid 32509825)
52. Drew, P.J. & Feldman, D.E. Intrinsic signal imaging of deprivation-induced contraction of whisker representations in rat somatosensory cortex. Cereb. Cortex 19, 331-348 (2009).
53. Foeller, E., Celikel, T. & Feldman, D.E. Inhibitory sharpening of receptive felds contributes to whisker map plasticity in rat somatosensory cortex. J. Neurophysiol. 94, 4387-4400 (2005). (Pubitemid 41691793)
54. Chen-Bee, C.H. et al. Visualizing and quantifying evoked cortical activity assessed with intrinsic signal imaging. J. Neurosci. Methods 97, 157-173 (2000). (Pubitemid 30219457)
55. Li, B. & Acton, S.T. Active contour external force using vector feld convolution for image segmentation. IEEE Trans. Image Process. 16, 2096-2106 (2007). (Pubitemid 47225461)
56. Jain, N. et al. Local-pooled-error test for identifying differentially expressed genes with a small number of replicated microarrays. Bioinformatics 19, 1945-1951 (2003). (Pubitemid 37322339)