Role of motor cortex NMDA receptors in learning-dependent synaptic plasticity of behaving mice

Nature Communications

Volumn 4, Issue , 2013, Pages

  Hasan, Mazahir T ^a,b   Hernández González, Samuel ^c   Dogbevia, Godwin ^a   Treviño, Mario ^a   Bertocchi, Ilaria ^a   Gruart, Agnès ^c   Delgado García, José M ^c  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1;

BIOCHEMISTRY; BRAIN; FUNCTIONAL ROLE; GENE EXPRESSION; LEARNING; NEUROLOGY; PHYSIOLOGY; RODENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE MEMORY; BRAIN CELL; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CONDITIONED REFLEX; CONTROLLED STUDY; CORNEA REFLEX; ELECTROMYOGRAPHY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; EYELID REFLEX; FEMALE; GENE DELETION; GENE EXPRESSION; IN SITU HYBRIDIZATION; IN VIVO STUDY; INSTRUMENTAL CONDITIONING; KNOCKOUT GENE; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY MOTOR CORTEX; PRIMARY SOMATOSENSORY CORTEX; RNA HYBRIDIZATION; STATE DEPENDENT LEARNING; SYNAPTIC EFFICACY; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING, OPERANT; ELECTROPHYSIOLOGICAL PHENOMENA; GENE DELETION; GENE KNOCKOUT TECHNIQUES; INTEGRASES; LEARNING; LONG-TERM POTENTIATION; MICE; MOTOR CORTEX; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; ORGAN SPECIFICITY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; TASK PERFORMANCE AND ANALYSIS;

EID: 84883309509     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3258     Document Type: Article

References (60)

1. Sanes, J. N. & Donoghue, J. P. Plasticity and primary motor cortex. Annu. Rev. Neurosci. 23, 393-415 (2000). (Pubitemid 30350048)
2. Hubel, D. H. & Wiesel, T. N. Receptive fields of single neurones in the cat?s striate cortex. J. Physiol. 148, 574-591 (1959).
3. Mountcastle, V. B. Modality and topographic properties of single neurons of cat?s somatic sensory cortex. J. Neurophysiol. 20, 408-434 (1957).
4. Buonomano, D. V. & Merzenich, M. M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149-186 (1998). (Pubitemid 28150662)
5. Rioult-Pedotti, M. S., Friedman, D., Donoghue, J. P. & Learning-induced, L. T. P. in neocortex. Science 290, 533-536 (2000).
6. Margolis, D. J. et al. Reorganization of cortical population activity imaged throughout long-term sensory deprivation. Nat. Neurosci. 15, 1539-1546 (2012).
7. Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473-478 (2012).
8. Hebb, D. O. The Organization of Behavior: A Neuropsychological Theory (Wiley and Sons, 1949).
9. Buzsaki, G. Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68, 362-385 (2010).
10. Callaway, E. M. Feedforward, feedback and inhibitory connections in primate visual cortex. Neural. Netw. 17, 625-632 (2004). (Pubitemid 39118310)
11. Aronoff, R. et al. Long-range connectivity of mouse primary somatosensory barrel cortex. Eur. J. Neurosci. 31, 2221-2233 (2010).
12. Ferezou, I. et al. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56, 907-923 (2007). (Pubitemid 350181347)
13. Larkum, M. E., Nevian, T., Sandler, M., Polsky, A. & Schiller, J. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325, 756-760 (2009).
14. Xu, N. L. et al. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492, 247-251 (2012).
15. McCormick, D. A. & Thompson, R. F. Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223, 296-299 (1984). (Pubitemid 14215791)
16. Gruart, A., Munoz, M. D. & Delgado-Garcia, J. M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J. Neurosci. 26, 1077-1087 (2006). (Pubitemid 43237039)
17. Moyer, Jr J. R., Thompson, L. T. & Disterhoft, J. F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. 16, 5536-5546 (1996). (Pubitemid 26277881)
18. Troncoso, J., Munera, A. & Delgado-Garcia, J. M. Learning-dependent potentiation in the vibrissal motor cortex is closely related to the acquisition of conditioned whisker responses in behaving mice. Learn. Mem. 14, 84-93 (2007). (Pubitemid 46203570)
19. Weible, A. P., McEchron, M. D. & Disterhoft, J. F. Cortical involvement in acquisition and extinction of trace eyeblink conditioning. Behav. Neurosci. 114, 1058-1067 (2000). (Pubitemid 32001885)
20. Karni, A. et al. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc. Natl Acad. Sci. USA 95, 861-868 (1998).
21. Kleim, J. A. et al. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 24, 628-633 (2004). (Pubitemid 38166488)
22. Komiyama, T. et al. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464, 1182-1186 (2010).
23. Kleim, J. A., Lussnig, E., Schwarz, E. R., Comery, T. A. & Greenough, W. T. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci. 16, 4529-4535 (1996). (Pubitemid 26242294)
24. Xu, T. et al. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462, 915-919 (2009).
25. Kleim, J. A. et al. Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn. Mem. 77, 63-77 (2002). (Pubitemid 34971544)
26. Hess, G. & Donoghue, J. P. Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J. Neurophysiol. 71, 2543-2547 (1994). (Pubitemid 24184887)
27. Rioult-Pedotti, M. S., Friedman, D., Hess, G. & Donoghue, J. P. Strengthening of horizontal cortical connections following skill learning. Nat. Neurosci. 1, 230-234 (1998).
28. Hess, G., Jacobs, K. M. & Donoghue, J. P. N-methyl-D-aspartate receptor mediated component of field potentials evoked in horizontal pathways of rat motor cortex. Neuroscience 61, 225-235 (1994).
29. Iwasato, T. et al. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726-731 (2000).
30. Kishimoto, Y. et al. Conditioned eyeblink response is impaired in mutant mice lacking NMDA receptor subunit NR2A. Neuroreport 8, 3717-3721 (1997). (Pubitemid 28004862)
31. Takatsuki, K., Kawahara, S., Takehara, K., Kishimoto, Y. & Kirino, Y. Effects of the noncompetitive NMDA receptor antagonist MK-801 on classical eyeblink conditioning in mice. Neuropharmacology 41, 618-628 (2001). (Pubitemid 32924972)
32. Kishimoto, Y., Kawahara, S., Mori, H., Mishina, M. & Kirino, Y. Long-trace interval eyeblink conditioning is impaired in mutant mice lacking the NMDA receptor subunit epsilon 1. Eur. J. Neurosci. 13, 1221-1227 (2001). (Pubitemid 32275759)
33. Niewoehner, B. et al. Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur. J. Neurosci. 25, 837-846 (2007).
34. Zhu, P. et al. Silencing and un-silencing of tetracycline-controlled genes in neurons. PLoS One 2, e533 (2007).
35. Cambridge, S. B. et al. Doxycycline-dependent photoactivated gene expression in eukaryotic systems. Nat. Methods 6, 527-531 (2009).
36. 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 (2000).
37. Burger, C., Nguyen, F. N., Deng, J. & Mandel, R. J. Systemic mannitol-induced hyperosmolality amplifies rAAV2-mediated striatal transduction to a greater extent than local co-infusion. Mol. Ther. 11, 327-331 (2004).
38. Madronal, N., Gruart, A. & Delgado-Garcia, J. M. Differing presynaptic contributions to LTP and associative learning in behaving mice. Front. Behav. Neurosci. 3, 7 (2009).
39. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002). (Pubitemid 34259234)
40. Lutcke, H. et al. Optical recording of neuronal activity with a geneticallyencoded calcium indicator in anesthetized and freely moving mice. Front. Neural. Circuits 4, 9 (2010).
41. Wallace, D. J. et al. Single-spike detection in vitro and in vivo with a genetic Ca2? sensor. Nat. Methods 5, 797-804 (2008).
42. Rokni, U., Richardson, A. G., Bizzi, E. & Seung, H. S. Motor learning with unstable neural representations. Neuron 54, 653-666 (2007). (Pubitemid 46756141)
43. Takiyama, K. & Okada, M. Maximization of learning speed in the motor cortex due to neuronal redundancy. PLoS Comput. Biol. 8, e1002348 (2012).
44. Woodruff-Pak, D. S. & Disterhoft, J. F. Where is the trace in trace conditioning? Trends Neurosci. (2008; 31, 105-112.
45. Clark, R. E., Manns, J. R. & Squire, L. R. Trace and delay eyeblink conditioning: contrasting phenomena of declarative and nondeclarative memory. Psychol. Sci. 12, 304-308 (2001). (Pubitemid 33653286)
46. Cheng, D. T., Disterhoft, J. F., Power, J. M., Ellis, D. A. & Desmond, J. E. Neural substrates underlying human delay and trace eyeblink conditioning. Proc. Natl Acad. Sci. USA 105, 8108-8113 (2008). (Pubitemid 351904716)
47. Fuster, J. M. Cortex and memory: emergence of a new paradigm. J. Cogn. Neurosci. 21, 2047-2072 (2009).
48. Clark, R. E. Eyeblink conditioning and systems consolidation: an ironic yet powerful pairing. Neurobiol. Learn. Mem. 95, 118-124 (2011).
49. Tsien, J. Z., Huerta, P. T. & Tonegawa, S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87, 1327-1338 (1996). (Pubitemid 27010115)
50. Huerta, P. T., Sun, L. D., Wilson, M. A. & Tonegawa, S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25, 473-480 (2000).
51. Fukaya, M., Kato, A., Lovett, C., Tonegawa, S. & Watanabe, M. Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc. Natl Acad. Sci. USA 100, 4855-4860 (2003). (Pubitemid 36457818)
52. Bannerman, D. M. et al. Dissecting spatial knowledge from spatial choice by hippocampal NMDA receptor deletion. Nat. Neurosci. 15, 1153-1159 (2012).
53. Kishimoto, Y., Nakazawa, K., Tonegawa, S., Kirino, Y. & Kano, M. Hippocampal CA3 NMDA receptors are crucial for adaptive timing of trace eyeblink conditioned response. J. Neurosci. 26, 1562-1570 (2006). (Pubitemid 43237026)
54. Osada, T., Adachi, Y., Kimura, H. M. & Miyashita, Y. Towards understanding of the cortical network underlying associative memory. Philos. Trans. R Soc. Lond. B Biol. Sci. 363, 2187-2199 (2008). (Pubitemid 351693533)
55. Miyamoto, K. et al. Functional differentiation of memory retrieval network in macaque posterior parietal cortex. Neuron 77, 787-799 (2013).
56. Moyer, Jr J. R., Deyo, R. A. & Disterhoft, J. F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosci. 104, 243-252 (1990). (Pubitemid 20168862)
57. Sprengel, R. & Hasan, M. T. Tetracycline-controlled genetic switches. Handb. Exp. Pharmacol. 178, 49-72 (2007).
58. Gureviciene, I. et al. Normal induction but accelerated decay of LTP in APP?PS1 transgenic mice. Neurobiol. Dis. 15, 188-195 (2004). (Pubitemid 38296749)
59. Bliss, T. V. & Gardner-Medwin, A. R. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J. Physiol. 232, 357-374 (1973).
60. Porras-Garcia, E., Cendelin, J., Dominguez-del-Toro, E., Vozeh, F. & Delgado-Garcia, J. M. Purkinje cell loss affects differentially the execution, acquisition and prepulse inhibition of skeletal and facial motor responses in Lurcher mice. Eur. J. Neurosci. 21, 979-988 (2005). (Pubitemid 40461051)