Arc regulates experience-dependent persistent firing patterns in frontal cortex

Journal of Neuroscience

Volumn 34, Issue 19, 2014, Pages 6583-6595

  Ren, Ming ^a   Cao, Vania ^a   Ye, Yizhou ^a   Manji, Husseini K ^a,b   Wang, Kuan Hong ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

Arc Arg3.1; Experience dependent; Frontal cortex; NMDA receptor; Persistent activity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; AMPA RECEPTOR; BICUCULLINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; DOPAMINE; DYNAMIN; ENDOPHILIN; GLUTAMATE RECEPTOR; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN DEPTH STIMULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE MICROSCOPY; FRONTAL CORTEX; GENE EXPRESSION; GENE EXPRESSION REGULATION; MEMBRANE DEPOLARIZATION; MOTOR ACTIVITY; MOUSE; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE; TASK PERFORMANCE;

ARC/ARG3.1; EXPERIENCE DEPENDENT; FRONTAL CORTEX; NMDA RECEPTOR; PERSISTENT ACTIVITY;

ACTION POTENTIALS; ANIMALS; BICUCULLINE; CELL MEMBRANE; CYTOSKELETAL PROTEINS; ELECTROPHYSIOLOGICAL PROCESSES; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GREEN FLUORESCENT PROTEINS; LEARNING; MICE; MICE, INBRED C57BL; MOTOR SKILLS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; POSTURAL BALANCE; PREFRONTAL CORTEX; RECEPTORS, AMPA;

EID: 84899845231     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0167-14.2014     Document Type: Article

References (53)

1. Barth AL (2007) Visualizing circuits and systems using transgenic reporters of neural activity. Curr Opin Neurobiol 17: 567-571. CrossRef Medline
2. Barth AL, Poulet JF (2012) Experimental evidence for sparse firing in the neocortex. Trends Neurosci 35: 345-355. CrossRef Medline
3. Barth AL, Gerkin RC, Dean KL (2004) Alteration of neuronal firing properties after in vivo experience in a FosGFP transgenic mouse. J Neurosci 24: 6466-6475. CrossRef Medline
4. Bramham CR, Worley PF, Moore MJ, Guzowski JF (2008) The immediate early gene arc/arg3. 1: regulation, mechanisms, and function. J Neurosci 28: 11760-11767. CrossRef Medline
5. Buitrago MM, Schulz JB, Dichgans J, Luft AR (2004) Short and long-term motor skill learning in an accelerated rotarod training paradigm. Neurobiol Learn Mem 81: 211-216. CrossRef Medline
6. Castner SA, Williams GV (2007) Tuning the engine of cognition: a focus on NMDA/D1 receptor interactions in prefrontal cortex. Brain Cogn 63: 94-122. CrossRef Medline
7. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3. 1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52: 445-459. CrossRef Medline
8. Costa RM, Cohen D, Nicolelis MA (2004) Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr Biol 14: 1124-1134. CrossRef Medline
9. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28: 771-784. CrossRef Medline
10. Durstewitz D, Gabriel T (2007) Dynamical basis of irregular spiking in NMDA-driven prefrontal cortex neurons. Cereb Cortex 17: 894-908. Medline
11. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178. CrossRef Medline
12. Erlich JC, Bialek M, Brody CD (2011) A cortical substrate for memoryguided orienting in the rat. Neuron 72: 330-343. CrossRef Medline
13. Farr TD, Liu L, Colwell KL, Whishaw IQ, Metz GA (2006) Bilateral alteration in stepping pattern after unilateral motor cortex injury: a new test strategy for analysis of skilled limb movements in neurological mouse models. J Neurosci Methods 153: 104-113. CrossRef Medline
14. Fromer M, Pocklington AJ, Kavanagh DH, Williams HJ, Dwyer S, Gormley P, Georgieva L, Rees E, Palta P, Ruderfer DM, Carrera N, Humphreys I, Johnson JS, Roussos P, Barker DD, Banks E, Milanova V, Grant SG, Hannon E, Rose SA, et al. (2014) De novo mutations in schizophrenia implicate synaptic networks. Nature 506: 179-184. CrossRef Medline
15. Fuster JM (1973) Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol 36: 61-78. Medline
16. Fuster JM (2001) The prefrontal cortex-an update: time is of the essence. Neuron 30: 319-333. CrossRef Medline
17. Guenthner CJ, Miyamichi K, Yang HH, Heller HC, Luo L (2013) Permanent genetic access to transiently active neurons via TRAP: targeted recombination in active populations. Neuron 78: 773-784. CrossRef Medline
18. Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA (2005) Mapping behaviorally relevant neural circuits with immediateearly gene expression. Curr Opin Neurobiol 15: 599-606. CrossRef Medline
19. Hahn TT, McFarland JM, Berberich S, Sakmann B, MehtaMR (2012) Spontaneous persistent activity in entorhinal cortex modulates corticohippocampal interaction in vivo. Nat Neurosci 15: 1531-1538. CrossRef Medline
20. Haider B, McCormick DA (2009) Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62: 171-189. CrossRef Medline
21. Histed MH, Pasupathy A, Miller EK (2009) Learning substrates in the primate prefrontal cortex and striatum: sustained activity related to successful actions. Neuron 63: 244-253. CrossRef Medline
22. Holschneider DP, Maarek JM, Yang J, Harimoto J, Scremin OU (2003) Functional brain mapping in freely moving rats during treadmill walking. J Cereb Blood Flow Metab 23: 925-932. Medline
23. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3: 661-669. CrossRef Medline
24. Jackson ME, Homayoun H, Moghaddam B (2004) NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci U S A 101: 8467-8472. CrossRef Medline
25. Jakkamsetti V, Tsai NP, Gross C, Molinaro G, Collins KA, Nicoletti F, Wang KH, Osten P, Bassell GJ, Gibson JR, Huber KM (2013) Experienceinduced Arc/Arg3. 1 primes CA1 pyramidal neurons for metabotropic glutamate receptor-dependent long-term synaptic depression. Neuron 80: 72-79. CrossRef Medline
26. Lewis DA, González-Burgos G (2008) Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology 33: 141-165. CrossRef Medline
27. Luscher C, Malenka RC (2012) NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 4 pii: a005710. CrossRef Medline
28. Major G, Tank D (2004) Persistent neural activity: prevalence and mechanisms. Curr Opin Neurobiol 14: 675-684. CrossRef Medline
29. Meyer-Lindenberg A, Weinberger DR (2006) Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev Neurosci 7: 818-827. CrossRef Medline
30. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24: 167-202. CrossRef Medline
31. Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M, Natsume R, Chowdhury S, Sakimura K, Worley PF, Bito H (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3. 1 with CaMKIIbeta. Cell 149: 886-898. CrossRef Medline
32. Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, Finkbeiner S (2010) Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci U S A 107: 18173-18178. CrossRef Medline
33. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, et al. (2006) Arc/Arg3. 1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444. CrossRef Medline
34. Purcell SM, Moran JL, Fromer M, Ruderfer D, Solovieff N, Roussos P, O'Dushlaine C, Chambert K, Bergen SE, Kähler A, Duncan L, Stahl E, Genovese G, Fernández E, Collins MO, Komiyama NH, Choudhary JS, Magnusson PK, Banks E, Shakir K, et al. (2014) A polygenic burden of rare disruptive mutations in schizophrenia. Nature 506: 185-190. CrossRef Medline
35. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT (2006) Increased expression of the immediate-early gene arc/arg3. 1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52: 461-474. CrossRef Medline
36. Sah P, Hestrin S, Nicoll RA (1989) Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science 246: 815-818. CrossRef Medline
37. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74: 1-58. CrossRef Medline
38. Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14: 279-284. CrossRef Medline
39. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423: 288-293. CrossRef Medline
40. Sidiropoulou K, Lu FM, Fowler MA, Xiao R, Phillips C, Ozkan ED, Zhu MX, White FJ, Cooper DC (2009) Dopamine modulates an mGluR5-mediated depolarization underlying prefrontal persistent activity. Nat Neurosci 12: 190-199. CrossRef Medline
41. Silva AJ, Zhou Y, Rogerson T, Shobe J, Balaji J (2009) Molecular and cellular approaches to memory allocation in neural circuits. Science 326: 391-395. CrossRef Medline
42. Stewart CV, Plenz D (2006) Inverted-U profile of dopamine-NMDAmediated spontaneous avalanche recurrence in superficial layers of rat prefrontal cortex. J Neurosci 26: 8148-8159. CrossRef Medline
43. Stuber GD, Klanker M, de Ridder B, Bowers MS, Joosten RN, Feenstra MG, Bonci A (2008) Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 321: 1690-1692. CrossRef Medline
44. Suh YH, Terashima A, Petralia RS, Wenthold RJ, Isaac JT, Roche KW, Roche PA (2010) A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking. Nat Neurosci 13: 338-343. CrossRef Medline
45. Takehara-Nishiuchi K, McNaughton BL (2008) Spontaneous changes of neocortical code for associative memory during consolidation. Science 322: 960-963. CrossRef Medline
46. Thuault SJ, Malleret G, Constantinople CM, Nicholls R, Chen I, Zhu J, Panteleyev A, Vronskaya S, Nolan MF, Bruno R, Siegelbaum SA, Kandel ER (2013) Prefrontal cortex HCN1 channels enable intrinsic persistent neural firing and executive memory function. J Neurosci 33: 13583-13599. CrossRef Medline
47. Tseng KY, O'Donnell P (2005) Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cereb Cortex 15: 49-57. Medline
48. Vazdarjanova A, Ramirez-Amaya V, Insel N, Plummer TK, Rosi S, Chowdhury S, Mikhael D, Worley PF, Guzowski JF, Barnes CA (2006) Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol 498: 317-329. CrossRef Medline
49. Wang KH, Majewska A, Schummers J, Farley B, Hu C, Sur M, Tonegawa S (2006) In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell 126: 389-402. CrossRef Medline
50. Wang M, Yang Y, Wang CJ, Gamo NJ, Jin LE, Mazer JA, Morrison JH, Wang XJ, Arnsten AF (2013) NMDA receptors subserve persistent neuronal firing during working memory in dorsolateral prefrontal cortex. Neuron 77: 736-749. CrossRef Medline
51. Wang XJ (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24: 455-463. CrossRef Medline
52. Williams GV, Goldman-Rakic PS (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376: 572-575. CrossRef Medline
53. Yassin L, Benedetti BL, Jouhanneau JS, Wen JA, Poulet JF, Barth AL (2010) An embedded subnetwork of highly active neurons in the neocortex. Neuron 68: 1043-1050. CrossRef Medline