Input- and Output-Specific Regulation of Serial Order Performance by Corticostriatal Circuits

Neuron

Volumn 88, Issue 2, 2015, Pages 345-356

  Rothwell, Patrick E ^a,b   Hayton, Scott J ^a,c   Sun, Gordon L ^a   Fuccillo, Marc V ^a,d   Lim, Byung Kook ^a,e   Malenka, Robert C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c MCKINSEY AND COMPANY   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Basal ganglia; Circuit; Medium spiny neuron; Motor cortex; Mouse; Optogenetics; Serial order; Striatum; Synaptic plasticity

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DORSOLATERAL STRIATUM; EXCITATORY POSTSYNAPTIC POTENTIAL; LEARNING; MALE; MOTOR CORTEX; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SERIAL ORDER TASK; SIGNAL TRANSDUCTION; TASK PERFORMANCE; ANIMAL; C57BL MOUSE; CORPUS STRIATUM; NERVE CELL NETWORK; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CORPUS STRIATUM; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR CORTEX; NERVE NET; NEURONAL PLASTICITY;

EID: 84944876283     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.09.035     Document Type: Article

References (58)

1. Agostino R., Berardelli A., Formica A., Accornero N., Manfredi M. Sequential arm movements in patients with Parkinson's disease, Huntington's disease and dystonia. Brain 1992, 115:1481-1495.
2. Ahmad M., Polepalli J.S., Goswami D., Yang X., Kaeser-Woo Y.J., Südhof T.C., Malenka R.C. Postsynaptic complexin controls AMPA receptor exocytosis during LTP. Neuron 2012, 73:260-267.
3. Akil H., Brenner S., Kandel E., Kendler K.S., King M.C., Scolnick E., Watson J.D., Zoghbi H.Y. Medicine. The future of psychiatric research: genomes and neural circuits. Science 2010, 327:1580-1581.
4. Aldridge J.W., Berridge K.C. Coding of serial order by neostriatal neurons: a "natural action" approach to movement sequence. J. Neurosci. 1998, 18:2777-2787.
5. Bailey K.R., Mair R.G. The role of striatum in initiation and execution of learned action sequences in rats. J. Neurosci. 2006, 26:1016-1025.
6. Bailey K.R., Mair R.G. Effects of frontal cortex lesions on action sequence learning in the rat. Eur. J. Neurosci. 2007, 25:2905-2915.
7. Belin D., Everitt B.J. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 2008, 57:432-441.
8. Benecke R., Rothwell J.C., Dick J.P., Day B.L., Marsden C.D. Disturbance of sequential movements in patients with Parkinson's disease. Brain 1987, 110:361-379.
9. Burguière E., Monteiro P., Feng G., Graybiel A.M. Optogenetic stimulation of lateral orbitofronto-striatal pathway suppresses compulsive behaviors. Science 2013, 340:1243-1246.
10. Burguière E., Monteiro P., Mallet L., Feng G., Graybiel A.M. Striatal circuits, habits, and implications for obsessive-compulsive disorder. Curr. Opin. Neurobiol. 2015, 30:59-65.
11. Cao V.Y., Ye Y., Mastwal S., Ren M., Coon M., Liu Q., Costa R.M., Wang K.H. Motor Learning Consolidates Arc-Expressing Neuronal Ensembles in Secondary Motor Cortex. Neuron 2015, 86:1385-1392.
12. Castañé A., Theobald D.E., Robbins T.W. Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats. Behav. Brain Res. 2010, 210:74-83.
13. Cui G., Jun S.B., Jin X., Pham M.D., Vogel S.S., Lovinger D.M., Costa R.M. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 2013, 494:238-242.
14. Dang M.T., Yokoi F., Yin H.H., Lovinger D.M., Wang Y., Li Y. Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum. Proc. Natl. Acad. Sci. USA 2006, 103:15254-15259.
15. Desrochers T.M., Amemori K., Graybiel A.M. Habit Learning by Naive Macaques Is Marked by Response Sharpening of Striatal Neurons Representing the Cost and Outcome of Acquired Action Sequences. Neuron 2015, 87:853-868.
16. Dölen G., Darvishzadeh A., Huang K.W., Malenka R.C. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013, 501:179-184.
17. Durieux P.F., Schiffmann S.N., de Kerchove d'Exaerde A. Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J. 2012, 31:640-653.
18. Erlich J.C., Bialek M., Brody C.D. A cortical substrate for memory-guided orienting in the rat. Neuron 2011, 72:330-343.
19. Fujii N., Graybiel A.M. Representation of action sequence boundaries by macaque prefrontal cortical neurons. Science 2003, 301:1246-1249.
20. Gerfen C.R., Surmeier D.J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 2011, 34:441-466.
21. Gerfen C.R., Paletzki R., Heintz N. GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 2013, 80:1368-1383.
22. Gittis A.H., Hang G.B., LaDow E.S., Shoenfeld L.R., Atallah B.V., Finkbeiner S., Kreitzer A.C. Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 2011, 71:858-868.
23. Gourley S.L., Lee A.S., Howell J.L., Pittenger C., Taylor J.R. Dissociable regulation of instrumental action within mouse prefrontal cortex. Eur. J. Neurosci. 2010, 32:1726-1734.
24. Graybiel A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 2008, 31:359-387.
25. 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 2014, 81:179-194.
26. Hodos W. Progressive ratio as a measure of reward strength. Science 1961, 134:943-944.
27. Jin X., Costa R.M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 2010, 466:457-462.
28. Jin X., Tecuapetla F., Costa R.M. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat. Neurosci. 2014, 17:423-430.
29. Jurado S., Goswami D., Zhang Y., Molina A.J., Südhof T.C., Malenka R.C. LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 2013, 77:542-558.
30. Kauer J.A., Malenka R.C. Synaptic plasticity and addiction. Nat. Rev. Neurosci. 2007, 8:844-858.
31. Koralek A.C., Jin X., Long J.D., Costa R.M., Carmena J.M. Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature 2012, 483:331-335.
32. Koralek A.C., Costa R.M., Carmena J.M. Temporally precise cell-specific coherence develops in corticostriatal networks during learning. Neuron 2013, 79:865-872.
33. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
34. Kreitzer A.C., Malenka R.C. Striatal plasticity and basal ganglia circuit function. Neuron 2008, 60:543-554.
35. Lashley K.S. The problem of serial order in behavior. Cerebral Mechanisms in Behavior 1951, 112-146. Wiley. L.A. Jeffress (Ed.).
36. Lerner T.N., Shilyansky C., Davidson T.J., Evans K.E., Beier K.T., Zalocusky K.A., Crow A.K., Malenka R.C., Luo L., Tomer R., Deisseroth K. Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits. Cell 2015, 162:635-647.
37. Lin J.Y., Lin M.Z., Steinbach P., Tsien R.Y. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 2009, 96:1803-1814.
38. Lin C.W., Sim S., Ainsworth A., Okada M., Kelsch W., Lois C. Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 2010, 65:32-39.
39. Lu X., Matsuzawa M., Hikosaka O. A neural correlate of oculomotor sequences in supplementary eye field. Neuron 2002, 34:317-325.
40. Luo L., Callaway E.M., Svoboda K. Genetic dissection of neural circuits. Neuron 2008, 57:634-660.
41. Murakami M., Vicente M.I., Costa G.M., Mainen Z.F. Neural antecedents of self-initiated actions in secondary motor cortex. Nat. Neurosci. 2014, 17:1574-1582.
42. Oldenburg I.A., Sabatini B.L. Antagonistic but Not Symmetric Regulation of Primary Motor Cortex by Basal Ganglia Direct and Indirect Pathways. Neuron 2015, 86:1174-1181.
43. Ostlund S.B., Winterbauer N.E., Balleine B.W. Evidence of action sequence chunking in goal-directed instrumental conditioning and its dependence on the dorsomedial prefrontal cortex. J. Neurosci. 2009, 29:8280-8287.
44. Reep R.L., Corwin J.V., Hashimoto A., Watson R.T. Efferent connections of the rostral portion of medial agranular cortex in rats. Brain Res. Bull. 1987, 19:203-221.
45. Rothwell P.E., Fuccillo M.V., Maxeiner S., Hayton S.J., Gokce O., Lim B.K., Fowler S.C., Malenka R.C., Südhof T.C. Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors. Cell 2014, 158:198-212.
46. Schiffmann S.N., Vanderhaeghen J.J. Adenosine A2 receptors regulate the gene expression of striatopallidal and striatonigral neurons. J. Neurosci. 1993, 13:1080-1087.
47. Schreiweis C., Bornschein U., Burguière E., Kerimoglu C., Schreiter S., Dannemann M., Goyal S., Rea E., French C.A., Puliyadi R., et al. Humanized Foxp2 accelerates learning by enhancing transitions from declarative to procedural performance. Proc. Natl. Acad. Sci. USA 2014, 111:14253-14258.
48. Schwartz N., Temkin P., Jurado S., Lim B.K., Heifets B.D., Polepalli J.S., Malenka R.C. Chronic pain. Decreased motivation during chronic pain requires long-term depression in the nucleus accumbens. Science 2014, 345:535-542.
49. Stuesse S.L., Newman D.B. Projections from the medial agranular cortex to brain stem visuomotor centers in rats. Exp. Brain Res. 1990, 80:532-544.
50. Taverna S., Ilijic E., Surmeier D.J. Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease. J. Neurosci. 2008, 28:5504-5512.
51. Thorn C.A., Atallah H., Howe M., Graybiel A.M. Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 2010, 66:781-795.
52. Wall N.R., De La Parra M., Callaway E.M., Kreitzer A.C. Differential innervation of direct- and indirect-pathway striatal projection neurons. Neuron 2013, 79:347-360.
53. Wickersham I.R., Finke S., Conzelmann K.K., Callaway E.M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 2007, 4:47-49.
54. Xiong Q., Znamenskiy P., Zador A.M. Selective corticostriatal plasticity during acquisition of an auditory discrimination task. Nature 2015, 521:348-351.
55. Yin H.H. The role of the murine motor cortex in action duration and order. Front. Integr. Nuerosci. 2009, 3:23.
56. Yin H.H. The sensorimotor striatum is necessary for serial order learning. J. Neurosci. 2010, 30:14719-14723.
57. Yin H.H., Mulcare S.P., Hilário M.R., Clouse E., Holloway T., Davis M.I., Hansson A.C., Lovinger D.M., Costa R.M. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 2009, 12:333-341.
58. Yizhar O., Fenno L.E., Davidson T.J., Mogri M., Deisseroth K. Optogenetics in neural systems. Neuron 2011, 71:9-34.