Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition

PLoS Computational Biology

Volumn 11, Issue 11, 2015, Pages

  Cannon, Jonathan ^a,b   Kopell, Nancy ^a   Gardner, Timothy ^a   Markowitz, Jeffrey ^a  

^a USA   (United States)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONS;

ARM MOVEMENTS; BEHAVIOR PROCESS; COGNITIVE PROCESS; FEED FORWARD; NEURAL ACTIVITY; REPRODUCIBLE BEHAVIOR; SEQUENCE GENERATION; SPATIOTEMPORAL PATTERNS; SYNFIRE CHAINS; THEORETICAL MODELING;

CHAINS;

DNA STRUCTURE; MODEL; NEGATIVE FEEDBACK; NERVOUS SYSTEM; TRAVEL; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; BIRD; COMPUTER SIMULATION; FEEDBACK SYSTEM; HUMAN; MOTOR CORTEX; NERVE CELL INHIBITION; PHYSIOLOGY;

ANIMALS; BIRDS; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; MODELS, NEUROLOGICAL; MOTOR CORTEX; NEURAL INHIBITION;

EID: 84949207746     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004581     Document Type: Article

References (42)

1. Hahnloser RHR, Kozhevnikov AA, Fee MS, (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419: 65–70. doi: 10.1038/nature00974 12214232
2. Long MA, Jin DZ, Fee MS, (2010) Support for a synaptic chain model of neuronal sequence generation. Nature 468: 394–399. doi: 10.1038/nature09514 20972420
3. Harvey CD, Coen P, Tank DW, (2012) Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484: 62–68. doi: 10.1038/nature10918 22419153
4. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G, (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321: 1322–1327. doi: 10.1126/science.1159775 18772431
5. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H, (2011) Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71: 737–749. doi: 10.1016/j.neuron.2011.07.012 21867888
6. Abeles M, (1991) Corticonics: Neural Circuits of the Cerebral Cortex. Cambridge University Press, first edition.
7. Diesmann M, Gewaltig MO, Aertsen A, (1999) Stable propagation of synchronous spiking in cortical neural networks. Nature 402: 529–533. doi: 10.1038/990101 10591212
8. Li M, Greenside H, (2006) Stable propagation of a burst through a one-dimensional homogeneous excitatory chain model of songbird nucleus HVC. Physical Review E 74(1): 011918. doi: 10.1103/PhysRevE.74.011918
9. Chang W, Jin D, (2009) Spike propagation in driven chain networks with dominant global inhibition. Physical Review E 79(5): 051917. doi: 10.1103/PhysRevE.79.051917
10. Jin DZ, (2009) Generating variable birdsong syllable sequences with branching chain networks in avian premotor nucleus HVC. Physical Review E 80(5): 051902. doi: 10.1103/PhysRevE.80.051902
11. Guitchounts G, Markowitz JE, Liberti W, Gardner TJ, (2013) A carbon-fiber electrode array for long-term neural recording. Journal of Neural Engineering 10(4): 046016. doi: 10.1088/1741-2560/10/4/046016 23860226
12. Kosche G, Vallentin D, Long M, (2015) Interplay of Inhibition and Excitation Shapes a Premotor Neural Sequence. Journal of Neuroscience 35(3):1217–1227. doi: 10.1523/JNEUROSCI.4346-14.2015 25609636
13. Markowitz JE, Liberti WA, Guitchounts G, Velho T, Lois C, Gardner TJ, (2015) Mesoscopic Patterns of Neural Activity Support Songbird Cortical Sequences. PLoS Biol 13(6): e1002158. doi: 10.1371/journal.pbio.1002158 26039895
14. Gibb L, Gentner TQ, Abarbanel HDI, (2009) Inhibition and recurrent excitation in a computational model of sparse bursting in song nucleus HVC. Journal of Neurophysiology 102: 1748–1762. doi: 10.1152/jn.00670.2007 19515949
15. Yildiz IB, Kiebel SJ, (2011) A hierarchical neuronal model for generation and online recognition of birdsongs. PLoS Computational Biology 7(12): e1002303. doi: 10.1371/journal.pcbi.1002303 22194676
16. Gibb L, Gentner TQ, Abarbanel HDI, (2009) Brain Stem Feedback in a Computational Model of Birdsong Sequencing. Journal of Neurophysiology 102(3): 1763–1778. doi: 10.1152/jn.91154.2008 19553477
17. Latham PE, Richmond BJ, Nelson PG, Nirenberg S, (2000) Intrinsic dynamics in neuronal networks. I. Theory. Journal of neurophysiology 83: 808–27. 10669496
18. De Almeida L, Idiart M, Lisman JE, (2009) A second function of gamma frequency oscillations: an E-percent-max winner-take-all mechanism selects which cells fire. Journal of Neuroscience, 29(23): 7497–503. doi: 10.1523/JNEUROSCI.6044-08.2009 19515917
19. Brandt SF, Wessel R, (2007) Winner-take-all selection in a neural system with delayed feedback. Biological Cybernetics, 97 (3): 221–228. doi: 10.1007/s00422-007-0168-y 17624546
20. Börgers C, Kopell NJ, (2003) Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity. Neural computation 538: 509–538.
21. Gewaltig M, Diesmann M, Aertsen A, (2001) Propagation of cortical synfire activity: survival probability in single trials and stability in the mean. Neural Networks 14: 657–73. doi: 10.1016/S0893-6080(01)00070-3 11665761
22. Rabinovich M, Volkovskii A, Lecanda P, Huerta R, Abarbanel HD, et al. (2001) Dynamical encoding by networks of competing neuron groups: winnerless competition. Physical Review Letters 87(6): 068102. doi: 10.1103/PhysRevLett.87.068102 11497865
23. Verduzco-Flores SO, Bodner M, Ermentrout GB, (2012) A model for complex sequence learning and reproduction in neural populations. Journal of Computational Neuroscience 32: 403–23. doi: 10.1007/s10827-011-0360-x 21887499
24. Assisi C, Stopfer M, Bazhenov M, (2011) Using the structure of inhibitory networks to unravel mechanisms of spatiotemporal patterning. Neuron 69(2): 373–386. doi: 10.1016/j.neuron.2010.12.019 21262473
25. Bertram R, Daou A, Hyson RL, Johnson F, Wu W, (2014) Two neural streams, one voice: Pathways for theme and variation in the songbird brain. Journal of Neuroscience 277: 806–817. doi: 10.1016/j.neuroscience.2014.07.061
26. Hanuschkin A, Diesmann M, Morrison A, (2011) A reafferent and feed-forward model of song syntax generation in the Bengalese finch. Journal of Computational Neuroscience 31(3): 509–32. doi: 10.1007/s10827-011-0318-z 21404048
27. Mooney R, Prather JF, (2005) The HVC Microcircuit: The Synaptic Basis for Interactions between Song Motor and Vocal Plasticity Pathways. Journal of Neuroscience 25: 1952–1964. doi: 10.1523/JNEUROSCI.3726-04.2005 15728835
28. Graber MH, Helmchen F, Hahnloser RHR, (2013) Activity in a premotor cortical nucleus of zebra finches is locally organized and exhibits auditory selectivity in neurons but not in glia. PloS one 8: e81177. doi: 10.1371/journal.pone.0081177 24312533
29. Day NF, Terleski KL, Nykamp DQ, Nick TA, (2013) Directed functional connectivity matures with motor learning in a cortical pattern generator. Journal of Neurophysiology 109: 913–923. doi: 10.1152/jn.00937.2012 23175804
30. Scott BB, Gardner T, Ji N, Fee MS, Lois C, (2012) Wandering neuronal migration in the postnatal vertebrate forebrain. Journal of Neuroscience 32: 1436–1446. doi: 10.1523/JNEUROSCI.2145-11.2012 22279228
31. Stauffer T, Elliott K, Ross M, Basista M, Hyson R, Johnson F, (2012) Axial organization of a brain region that sequences a learned pattern of behavior. Journal of Neuroscience 32(27): 9312–9322. doi: 10.1523/JNEUROSCI.0978-12.2012 22764238
32. Nottebohm F, Kelley DB, Paton JA, (1982) Connections of vocal control nuclei in the canary telencephalon. Journal of Comparative Neurology 207: 344–357. doi: 10.1002/cne.902070406 7119147
33. Kozhevnikov AA, Fee MS, (2007) Singing-related activity of identified HVC neurons in the zebra finch. Journal of Neurophysiology 97(6): 4271–4283. doi: 10.1152/jn.00952.2006 17182906
34. Goldman MS, (2009) Memory without Feedback in a Neural Network. Neuron, 61(4): 621–634. doi: 10.1016/j.neuron.2008.12.012 19249281
35. Liu JK, Buonomano DV, (2009) Embedding multiple trajectories in simulated recurrent neural networks in a self-organizing manner. Journal of Neuroscience, 29(42): 13172–81. doi: 10.1523/JNEUROSCI.2358-09.2009 19846705
36. Hahn G, Bujan AF, Frégnac Y, Aertsen A, Kumar A, (2014) Communication through resonance in spiking neuronal networks. PLoS Computational Biology 10(8): e1003811. doi: 10.1371/journal.pcbi.1003811 25165853
37. Jahnke S, Memmesheimer R-M, Timme M, (2014) Oscillation-Induced Signal Transmission and Gating in Neural Circuits. PLoS Computational Biology 10(12): e1003940. doi: 10.1371/journal.pcbi.1003940 25503492
38. Amador A, Perl YS, Mindlin GB, Margoliash D, (2013) Elemental gesture dynamics are encoded by song premotor cortical neurons. Nature 495: 59–64. doi: 10.1038/nature11967 23446354
39. Shmiel T, Drori R, Shmiel O, Ben-Shaul Y, Nadasdy Z, et al. (2006) Temporally precise cortical firing patterns are associated with distinct action segments. Journal of Neurophysiology 96: 2645–52. doi: 10.1152/jn.00798.2005 16885517
40. Lee AK, Wilson MA, (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36: 1183–94. doi: 10.1016/S0896-6273(02)01096-6 12495631
41. Rubino D, Robbins Ka, Hatsopoulos NG, (2006) Propagating waves mediate information transfer in the motor cortex. Nature neuroscience 9: 1549–57. doi: 10.1038/nn1802 17115042
42. Lubenov EV, Siapas AG, (2009) Hippocampal theta oscillations are travelling waves. Nature 459: 534–9. doi: 10.1038/nature08010 19489117