Population-Level Representation of a Temporal Sequence Underlying Song Production in the Zebra Finch

Neuron

Volumn 90, Issue 4, 2016, Pages 866-876

  Picardo, Michel A ^a,b   Merel, Josh ^c   Katlowitz, Kalman A ^a,b   Vallentin, Daniela ^a,b   Okobi, Daniel E ^a,b   Benezra, Sam E ^a,b   Clary, Rachel C ^a,b   Pnevmatikakis, Eftychios A ^c,d   Paninski, Liam ^c   Long, Michael A ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d Simons Center for Data Analysis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTICS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BAYES THEOREM; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CONTROLLED STUDY; FEMALE; FLUORESCENCE MICROSCOPY; INSTRUMENTAL CONDITIONING; INTERNEURON; LATENT PERIOD; LOCOMOTION; MALE; MOTONEURON NUCLEUS; MOTOR EVOKED POTENTIAL; NERVE CELL; NERVE PROJECTION; NONHUMAN; PHONATION; PREMOTOR CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SINGING; SYNAPTIC INHIBITION; TAENIOPYGIA GUTTATA; VOCALIZATION; WHOLE CELL PATCH CLAMP; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; FINCH; FOREBRAIN; PHYSIOLOGY; PROCEDURES;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; FEMALE; FINCHES; MALE; NEURONS; PROSENCEPHALON; VOCALIZATION, ANIMAL;

EID: 84968865159     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.02.016     Document Type: Article

References (62)

1. Abeles M. Corticonics: Neural Circuits of the Cerebral Cortex 1991, Cambridge University Press.
2. Amador A., Perl Y.S., Mindlin G.B., Margoliash D. Elemental gesture dynamics are encoded by song premotor cortical neurons. Nature 2013, 495:59-64.
3. Andalman A.S., Foerster J.N., Fee M.S. Control of vocal and respiratory patterns in birdsong: dissection of forebrain and brainstem mechanisms using temperature. PLoS ONE 2011, 6:e25461.
4. Ashmore R.C., Wild J.M., Schmidt M.F. Brainstem and forebrain contributions to the generation of learned motor behaviors for song. J. Neurosci. 2005, 25:8543-8554.
5. Boari S., Sanz Perl Y., Amador A., Margoliash D., Mindlin G.B. Automatic reconstruction of physiological gestures used in a model of birdsong production. J. Neurophysiol. 2015, 114:2912-2922.
6. Briggman K.L., Helmstaedter M., Denk W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 2011, 471:183-188.
7. Carpenter A.F., Georgopoulos A.P., Pellizzer G. Motor cortical encoding of serial order in a context-recall task. Science 1999, 283:1752-1757.
8. 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 2013, 499:295-300.
9. Churchland M.M., Cunningham J.P., Kaufman M.T., Foster J.D., Nuyujukian P., Ryu S.I., Shenoy K.V. Neural population dynamics during reaching. Nature 2012, 487:51-56.
10. Day N.F., Terleski K.L., Nykamp D.Q., Nick T.A. Directed functional connectivity matures with motor learning in a cortical pattern generator. J. Neurophysiol. 2013, 109:913-923.
11. Denk W., Strickler J.H., Webb W.W. Two-photon laser scanning fluorescence microscopy. Science 1990, 248:73-76.
12. Dombeck D.A., Harvey C.D., Tian L., Looger L.L., Tank D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 2010, 13:1433-1440.
13. Evarts E.V. Relation of pyramidal tract activity to force exerted during voluntary movement. J. Neurophysiol. 1968, 31:14-27.
14. Fee M.S., Kozhevnikov A.A., Hahnloser R.H. Neural mechanisms of vocal sequence generation in the songbird. Ann. N Y Acad. Sci. 2004, 1016:153-170.
15. Fiete I.R., Senn W., Wang C.Z., Hahnloser R.H. Spike-time-dependent plasticity and heterosynaptic competition organize networks to produce long scale-free sequences of neural activity. Neuron 2010, 65:563-576.
16. Garst-Orozco J., Babadi B., Ölveczky B.P. A neural circuit mechanism for regulating vocal variability during song learning in zebra finches. eLife 2014, 3:e03697.
17. Georgopoulos A.P., Schwartz A.B., Kettner R.E. Neuronal population coding of movement direction. Science 1986, 233:1416-1419.
18. Goller F., Cooper B.G. Peripheral motor dynamics of song production in the zebra finch. Ann. N Y Acad. Sci. 2004, 1016:130-152.
19. Graber M.H., Helmchen F., Hahnloser R.H. Activity in a premotor cortical nucleus of zebra finches is locally organized and exhibits auditory selectivity in neurons but not in glia. PLoS ONE 2013, 8:e81177.
20. Hahnloser R.H., Kozhevnikov A.A., Fee M.S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 2002, 419:65-70.
21. Hartley R.S., Suthers R.A. Airflow and pressure during canary song: direct evidence for mini-breaths. J. Comp. Physiol. A 1989, 165:15-26.
22. Harvey C.D., Coen P., Tank D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 2012, 484:62-68.
23. 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 2012, 484:473-478.
24. Jun J.K., Jin D.Z. Development of neural circuitry for precise temporal sequences through spontaneous activity, axon remodeling, and synaptic plasticity. PLoS ONE 2007, 2:e723.
25. Ko H., Hofer S.B., Pichler B., Buchanan K.A., Sjöström P.J., Mrsic-Flogel T.D. Functional specificity of local synaptic connections in neocortical networks. Nature 2011, 473:87-91.
26. Kosche G., Vallentin D., Long M.A. Interplay of inhibition and excitation shapes a premotor neural sequence. J. Neurosci. 2015, 35:1217-1227.
27. Kozhevnikov A.A., Fee M.S. Singing-related activity of identified HVC neurons in the zebra finch. J. Neurophysiol. 2007, 97:4271-4283.
28. Lenschow C., Brecht M. Barrel cortex membrane potential dynamics in social touch. Neuron 2015, 85:718-725.
29. Leonardo A., Fee M.S. Ensemble coding of vocal control in birdsong. J. Neurosci. 2005, 25:652-661.
30. Li N., Chen T.W., Guo Z.V., Gerfen C.R., Svoboda K. A motor cortex circuit for motor planning and movement. Nature 2015, 519:51-56.
31. Long M.A., Fee M.S. Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 2008, 456:189-194.
32. Long M.A., Jin D.Z., Fee M.S. Support for a synaptic chain model of neuronal sequence generation. Nature 2010, 468:394-399.
33. Lu X., Ashe J. Anticipatory activity in primary motor cortex codes memorized movement sequences. Neuron 2005, 45:967-973.
34. Lu X., Ashe J. Dynamic reorganization of neural activity in motor cortex during new sequence production. Eur. J. Neurosci. 2015, 42:2172-2178.
35. Markowitz J.E., Liberti W.A., Guitchounts G., Velho T., Lois C., Gardner T.J. Mesoscopic patterns of neural activity support songbird cortical sequences. PLoS Biol. 2015, 13:e1002158.
36. Matsuzaka Y., Picard N., Strick P.L. Skill representation in the primary motor cortex after long-term practice. J. Neurophysiol. 2007, 97:1819-1832.
37. Mello G.B., Soares S., Paton J.J. A scalable population code for time in the striatum. Curr. Biol. 2015, 25:1113-1122.
38. Méndez J.M., Dall'Asén A.G., Cooper B.G., Goller F. Acquisition of an acoustic template leads to refinement of song motor gestures. J. Neurophysiol. 2010, 104:984-993.
39. Mita A., Mushiake H., Shima K., Matsuzaka Y., Tanji J. Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat. Neurosci. 2009, 12:502-507.
40. Mooney R., Prather J.F. The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J. Neurosci. 2005, 25:1952-1964.
41. Nachev P., Coulthard E., Jäger H.R., Kennard C., Husain M. Enantiomorphic normalization of focally lesioned brains. Neuroimage 2008, 39:1215-1226.
42. Nottebohm F., Stokes T.M., Leonard C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 1976, 165:457-486.
43. Okubo T.S., Mackevicius E.L., Payne H.L., Lynch G.F., Fee M.S. Growth and splitting of neural sequences in songbird vocal development. Nature 2015, 528:352-357.
44. Oomura Y., Yoshimatsu H., Aou S. Medial preoptic and hypothalamic neuronal activity during sexual behavior of the male monkey. Brain Res. 1983, 266:340-343.
45. Pastalkova E., Itskov V., Amarasingham A., Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
46. Peh W.Y., Roberts T.F., Mooney R. Imaging auditory representations of song and syllables in populations of sensorimotor neurons essential to vocal communication. J. Neurosci. 2015, 35:5589-5605.
47. Perl Y.S., Arneodo E.M., Amador A., Goller F., Mindlin G.B. Reconstruction of physiological instructions from Zebra finch song. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2011, 84:051909.
48. Peters A.J., Chen S.X., Komiyama T. Emergence of reproducible spatiotemporal activity during motor learning. Nature 2014, 510:263-267.
49. Pologruto T.A., Sabatini B.L., Svoboda K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2003, 2:13.
50. Ravassard P., Kees A., Willers B., Ho D., Aharoni D., Cushman J., Aghajan Z.M., Mehta M.R. Multisensory control of hippocampal spatiotemporal selectivity. Science 2013, 340:1342-1346.
51. Riede T., Goller F. Functional morphology of the sound-generating labia in the syrinx of two songbird species. J. Anat. 2010, 216:23-36.
52. Sober S.J., Wohlgemuth M.J., Brainard M.S. Central contributions to acoustic variation in birdsong. J. Neurosci. 2008, 28:10370-10379.
53. Solis M.M., Perkel D.J. Rhythmic activity in a forebrain vocal control nucleus in vitro. J. Neurosci. 2005, 25:2811-2822.
54. Suthers R.A., Goller F., Hartley R.S. Motor dynamics of song production by mimic thrushes. J. Neurobiol. 1994, 25:917-936.
55. Tanji J., Shima K. Role for supplementary motor area cells in planning several movements ahead. Nature 1994, 371:413-416.
56. Todorov E. Direct cortical control of muscle activation in voluntary arm movements: a model. Nat. Neurosci. 2000, 3:391-398.
57. Troyer T.W. Neuroscience: The units of a song. Nature 2013, 495:56-57.
58. Vallentin D., Long M.A. Motor origin of precise synaptic inputs onto forebrain neurons driving a skilled behavior. J. Neurosci. 2015, 35:299-307.
59. Vicario D.S. Contributions of syringeal muscles to respiration and vocalization in the zebra finch. J. Neurobiol. 1991, 22:63-73.
60. Vicario D.S. Organization of the zebra finch song control system: II. Functional organization of outputs from nucleus Robustus archistriatalis. J. Comp. Neurol. 1991, 309:486-494.
61. Vu E.T., Mazurek M.E., Kuo Y.C. Identification of a forebrain motor programming network for the learned song of zebra finches. J. Neurosci. 1994, 14:6924-6934.
62. Yu A.C., Margoliash D. Temporal hierarchical control of singing in birds. Science 1996, 273:1871-1875.