Coordination of distinct motor structures through remote axonal coupling of projection interneurons

Journal of Neuroscience

Volumn 31, Issue 43, 2011, Pages 15438-15449

  Jing, Jian ^a   Sasaki, Kosei ^a   Perkins, Matthew H ^a   Siniscalchi, Michael J ^a   Ludwar, Bjoern C ^a   Cropper, Elizabeth C ^a   Weiss, Klaudiusz R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; APLYSIA; ARTICLE; CONTROLLED STUDY; FEEDING; INNERVATION; INTERNEURON; LIP; MOTONEURON; MOTOR COORDINATION; NERVE CELL STIMULATION; NERVE FIBER; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL;

ABLATION TECHNIQUES; ANIMALS; APLYSIA; AXONS; CEREBRAL CORTEX; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; FEEDBACK; FEEDING BEHAVIOR; FUNCTIONAL LATERALITY; HYDRAZINES; INTERNEURONS; MOTOR NEURONS; MOUTH; MOVEMENT; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 80054923664     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3741-11.2011     Document Type: Article

References (60)

1. Bartos M, Manor Y, Nadim F, Marder E, Nusbaum MP (1999) Coordination of fast and slow rhythmic neuronal circuits. J Neurosci 19:6650-6660.
2. Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495-511.
3. Briggman KL, Kristan WB (2008) Multifunctional pattern-generating circuits. Annu Rev Neurosci 31:271-294.
4. Chiel HJ, Weiss KR, Kupfermann I (1986) An identified histaminergic neuron modulates feeding motor circuitry in Aplysia. J Neurosci 6:2427-2450.
5. Church PJ, Lloyd PE (1994) Activity of multiple identified motor neurons recorded intracellularly during evoked feedinglike motor programs in Aplysia. J Neurophysiol 72:1794-1809.
6. Coleman MJ, Meyrand P, Nusbaum MP (1995) A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378:502-505.
7. Davis WJ, Kovac MP, Croll RP, Matera EM (1984) Brain oscillator(s) underlying rhythmic cerebral and buccal motor output in the mollusc, Pleurobranchaea californica. J Exp Biol 110:1-15.
8. Dembrow NC, Jing J, Brezina V, Weiss KR (2004) A specific synaptic pathway activates a conditional plateau potential underlying protraction phase in the Aplysia feeding central pattern generator. J Neurosci 24:5230-5238.
9. Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462-467.
10. Dietz V, Michel J (2009) Human bipeds use quadrupedal coordination during locomotion. Ann N Y Acad Sci 1164:97-103.
11. Edwards DH, Heitler WJ, Krasne FB (1999) Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci 22:153-161.
12. Evans CG, Jing J, Rosen SC, Cropper EC (2003) Regulation of spike initiation and propagation in an Aplysia sensory neuron: gating-in via central depolarization. J Neurosci 23:2920-2931.
13. Friedman AK, Zhurov Y, Ludwar BCh, Weiss KR (2009) Motor outputs in a multi-tasking network: relative contributions of inputs and experiencedependent states. J Neurophysiol 102:3711-3727.
14. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2:425-433.
15. Gariépy JF, Missaghi K, Dubuc R (2010) The interactions between locomotion and respiration. Prog Brain Res 187:173-188.
16. Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Handbook of physiology, Sec 1, Vol 2 (Brooks V, ed), pp 1179-1236.
17. Bethesda, MD: American Physiological Society
18. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751-766.
19. Harris-Warrick RM, Marder E, Selverston AI, Moulins M, eds (1992) Dynamic biological networks: the stomatogastric nervous system. Cambridge, MA: MIT Press.
20. Hill AA, Masino MA, Calabrese RL (2003) Intersegmental coordination of rhythmic motor patterns. J Neurophysiol 90:531-538.
21. Hurwitz I, Susswein AJ (1996) B64, a newly identified central pattern generator element producing a phase switch from protraction to retraction in buccal motor programs of Aplysia californica. J Neurophysiol 75:1327-1344.
22. Hurwitz I, Goldstein RS, Susswein AJ (1994) Compartmentalization of pattern-initiation and motor functions in the B31 and B32 neurons of the buccal ganglia of Aplysia californica. J Neurophysiol 71:1514-1527.
23. Hurwitz I, Kupfermann I, Susswein AJ (1997) Different roles of neurons B63 and B34 that are active during the protraction phase of buccal motor programs in Aplysia californica. J Neurophysiol 78:1305-1319.
24. Hurwitz I, Kupfermann I, Weiss KR (2003) Fast synaptic connections from CBIs to pattern-generating neurons in Aplysia: initiation and modification of motor programs. J Neurophysiol 89:2120-2136.
25. Jing J, Weiss KR (2001) Neural mechanisms of motor program switching in Aplysia. J Neurosci 21:7349-7362.
26. Jing J, Weiss KR (2002) Interneuronal basis of the generation of related but distinct motor programs in Aplysia: implications for current neuronal models of vertebrate intralimb coordination. J Neurosci 22:6228-6238.
27. Jing J, Weiss KR (2005) Generation of variants of a motor act in a modular and hierarchical motor network. Curr Biol 15:1712-1721.
28. Jing J, Vilim FS, Wu JS, Park JH, Weiss KR (2003) Concerted GABAergic actions of Aplysia feeding interneurons in motor program specification. J Neurosci 23:5283-5294.
29. Jing J, Cropper EC, Hurwitz I, Weiss KR (2004) The construction of movement with behavior-specific and behavior-independent modules. J Neurosci 24:6315-6325.
30. Jing J, Vilim FS, Horn CC, Alexeeva V, Hatcher NG, Sasaki K, Yashina I, Zhurov Y, Kupfermann I, Sweedler JV, Weiss KR (2007) From hunger to satiety: reconfiguration of a feeding network by Aplysia neuropeptide Y. J Neurosci 27:3490-3502.
31. Jing J, Gillette R, Weiss KR (2009) Evolving concepts of arousal: insights from simple model systems. Rev Neurosci 20:405-427.
32. Jing J, Sweedler JV, Cropper EC, Alexeeva V, Park JH, Romanova EV, Xie F, Dembrow NC, Ludwar BC, Weiss KR, Vilim FS (2010) Feedforward compensation mediated by the central and peripheral actions of a single neuropeptide discovered using representational difference analysis. J Neurosci 30:16545-16558.
33. Jinno S, Klausberger T, Marton LF, Dalezios Y, Roberts JD, Fuentealba P, Bushong EA, Henze D, Buzsáki G, Somogyi P (2007) Neuronal diversity in GABAergic long-range projections from the hippocampus. J Neurosci 27:8790-8804.
34. Korn H, Faber DS (2005) The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47:13-28.
35. Kristan WB Jr, Calabrese RL, Friesen WO (2005) Neuronal control of leech behavior. Prog Neurobiol 76:279-327.
36. Ludwar BCh, Göritz ML, Schmidt J (2005) Intersegmental coordination of walking movements in stick insects. J Neurophysiol 93:1255-1265.
37. Morgan PT, Jing J, Vilim FS, Weiss KR (2002) Interneuronal and peptidergic control of motor pattern switching in Aplysia. J Neurophysiol 87:49-61.
38. Morton DW, Chiel HJ (1993a) In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia. J Comp Physiol A 172:17-32.
39. Morton DW, Chiel HJ (1993b) The timing of activity in motor neurons that produce radula movements distinguishes ingestion from rejection in Aplysia. J Comp Physiol A 173:519-536.
40. Mullins OJ, Hackett JT, Buchanan JT, Friesen WO (2011) Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems. Prog Neurobiol 93:244-269.
41. Nadim F, Manor Y, Nusbaum MP, Marder E (1998) Frequency regulation of a slow rhythm by a fast periodic input. J Neurosci 18:5053-5067.
42. Nargeot R, Baxter DA, Byrne JH (1997) Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning. J Neurosci 17:8093-8105.
43. Nishikawa KC (1999) Neuromuscular control of prey capture in frogs. Philos Trans R Soc Lond B Biol Sci 354:941-954.
44. Nusbaum MP, Beenhakker MP (2002) A small-systems approach to motor pattern generation. Nature 417:343-350.
45. Perrins R, Weiss KR (1996) A cerebral central pattern generator in Aplysia and its connections with buccal feeding circuitry. J Neurosci 16:7030-7045.
46. Perrins R, Weiss KR (1998) Compartmentalization of information processing in an Aplysia feeding circuit interneuron through membrane properties and synaptic interactions. J Neurosci 18:3977-3989.
47. Proekt A, Brezina V, Weiss KR (2004) Dynamical basis of intentions and expectations in a simple neuronal network. Proc Natl Acad Sci U S A 101:9447-9452.
48. Proekt A, Jing J, Weiss KR (2007) Multiple contributions of an inputrepresenting neuron to the dynamics of the Aplysia feeding network. J Neurophysiol 97:3046-3056.
49. Rosen SC, Teyke T, Miller MW, Weiss KR, Kupfermann I (1991) Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. J Neurosci 11:3630-3655.
50. Rovainen CM (1979) Neurobiology of lampreys. Physiol Rev 59:1007-1077.
51. Sasaki K, Brezina V, Weiss KR, Jing J (2009) Distinct inhibitory neurons exert temporally specific control over activity of a motoneuron receiving concurrent excitation and inhibition. J Neurosci 29:11732-11744.
52. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
53. Smarandache C, Hall WM, Mulloney B (2009) Coordination of rhythmic motor activity by gradients of synaptic strength in a neural circuit that couples modular neural oscillators. J Neurosci 29:9351-9360.
54. Susswein AJ, Byrne JH (1988) Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia. J Neurosci 8:2049-2061.
55. Tamás G, Buhl EH, Lörincz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3:366-371.
56. Teyke T, Rosen SC, Weiss KR, Kupfermann I (1993) Dopaminergic neuron- B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia. Brain Res 630:226-237.
57. Weiss KR, Kupfermann I (1976) Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs. Brain Res 117:33-49.
58. Williams TL (1992) Phase coupling by synaptic spread in chains of coupled neuronal oscillators. Science 258:662-665.
59. Wu JS, Vilim FS, Hatcher NG, Due MR, Sweedler JV, Weiss KR, Jing J (2010) Composite modulatory feedforward loop contributes to the establishment of a network state. J Neurophysiol 103:2174-2184.
60. Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347-361.