An input-representing interneuron regulates spike timing and thereby phase switching in a motor network

Journal of Neuroscience

Volumn 28, Issue 8, 2008, Pages 1916-1928

  Sasaki, Kosei ^a   Jing, Jian ^a   Due, Michael R ^a   Weiss, Klaudiusz R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Aplysia; Central pattern generator; Feeding; Motor programs; Phase transition; Spike timing

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; APLYSIA; ARTICLE; CONTROLLED STUDY; HYPERPOLARIZATION; INTERNEURON; MOTOR PERFORMANCE; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; APLYSIA; FEEDING BEHAVIOR; GANGLIA, INVERTEBRATE; INTERNEURONS; MALE; MOTOR ACTIVITY; MOTOR NEURONS; NERVE NET;

EID: 39749148306     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4755-07.2008     Document Type: Article

References (57)

1. Ayali A, Harris-Warrick RM (1999) Monoamine control of the pacemaker kernel and cycle frequency in the lobster pyloric network. J Neurosci 19:6712-6722.
2. Bartos M, Nusbaum MP (1997) Intercircuit control of motor pattern modulation by presynaptic inhibition. J Neurosci 17:2247-2256.
3. Berkowitz A (2007) Spinal interneurons that are selectively activated during fictive flexion reflex. J Neurosci 27:4634-4641.
4. Berkowitz A, Stein PS (1994) Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses. J Neurosci 14:5105-5119.
5. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
6. Blitz DM, Christie AE, Coleman MJ, Norris BJ, Marder E, Nusbaum MP (1999) Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network. J Neurosci 19:5449-5463.
7. Briggman KL, Kristan Jr WB (2006) Imaging dedicated and multifunctional neural circuits generating distinct behaviors. J Neurosci 26:10925-10933.
8. Bucher D, Thirumalai V, Marder E (2003) Axonal dopamine receptors activate peripheral spike initiation in a stomatogastric motor neuron. J Neurosci 23:6866-6875.
9. Cassenaer S, Laurent G (2007) Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448:709-713.
10. Church PJ, Lloyd PE (1994) Activity of multiple identified motor neurons recorded intracellularly during evoked feeding-like motor programs in Aplysia. J Neurophysiol 72:1794-1809.
11. Combes D, Meyrand P, Simmers J (1999) Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. J Neurosci 19:3620-3628.
12. Dickinson PS, Mecsas C, Marder E (1990) Neuropeptide fusion of two motor-pattern generator circuits. Nature 344:155-158.
13. Due MR, Jing J, Weiss KR (2004) Dopaminergic contributions to modulatory functions of a dual-transmitter interneuron in Aplysia. Neurosci Lett 358:53-57.
14. Due MR, Alexeeva V, Jing J, Weiss KR, Vilim F (2005) Involvement of glutamate in specification of protraction phase duration in feeding motor programs of Aplysia. Soc Neurosci Abstr 31:177.10.
15. Getting PA (1989) Reconstruction of small neural networks. In: Methods in neuronal modeling (Koch C, Segev I, eds), pp 171-194. Cambridge, MA: MIT.
16. Getting PA, Dekin MS (1985) Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator. J Neurophysiol 53:466-480.
17. Heitler WJ (1985) Motor programme switching in the crayfish swimmeret system. J Exp Biol 114:521-549.
18. Hooper SL, Moulins M (1989) Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244:1587-1589.
19. 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.
20. 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.
21. Hurwitz I, Neustadter D, Morton DW, Chiel HJ, Susswein AJ (1996) Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica. J Neurophysiol 75:1309-1326.
22. Jing J, Gillette R (2003) Directional avoidance turns encoded by single interneurons and sustained by multifunctional serotonergic cells. J Neurosci 23:3039-3051.
23. Jing J, Weiss KR (2001) Neural mechanisms of motor program switching in Aplysia. J Neurosci 21:7349-7362.
24. Jing J, Weiss KR (2005) Generation of variants of a motor act in a modular and hierarchical motor network. Curr Biol 15:1712-1721.
25. 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.
26. 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.
27. Jing J, Vilim FS, Horn CC, Alexeeva V, Hatcher NG, Sasaki K, Yashina I, 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.
28. Kabotyanski EA, Baxter DA, Byrne JH (1998) Identification and characterization of catecholaminergic neuron B65, which initiates and modifies patterned activity in the buccal ganglia of Aplysia. J Neurophysiol 79:605-621.
29. Koh HY, Weiss KR (2007) Activity-dependent peptidergic modulation of the plateau-generating neuron B64 in the feeding network of Aplysia. J Neurophysiol 97:1862-1867.
30. Kristan Jr WB, Calabrese RL, Friesen WO (2005) Neuronal control of leech behavior. Prog Neurobiol 76:279-327.
31. Kupfermann I, Weiss KR (2001) Motor program selection in simple model systems. Curr Opin Neurobiol 11:673-677.
32. Lieske SP, Thoby-Brisson M, Telgkamp P, Ramirez JM (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat Neurosci 3:600-607.
33. Lum CS, Zhurov Y, Cropper EC, Weiss KR, Brezina V (2005) Variability of swallowing performance in intact, freely feeding Aplysia. J Neurophysiol 94:2427-2446.
34. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687-717.
35. Morgan PT, Jing J, Vilim FS, Weiss KR (2002) Interneuronal and peptidergic control of motor pattern switching in Aplysia. J Neurophysiol 87:49-61.
36. Morton DW, Chiel HJ (1993a) The timing of activity in motor neurons that produce radula movements distinguishes ingestion from rejection in Aplysia. J Comp Physiol 173:519-536.
37. Morton DW, Chiel HJ (1993b) In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia. J Comp Physiol 172:17-32.
38. Murphy GJ, Rieke F (2006) Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52:511-524.
39. 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.
40. 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.
41. Popescu IR, Frost WN (2002) Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22:1985-1993.
42. Proekt A, Brezina V, Weiss KR (2004) Dynamical basis of intentions and expectations in a simple neuronal network. Proc Natl Acad Sci USA 101:9447-9452.
43. Proekt A, Jing J, Weiss KR (2007) Multiple contributions of an input-representing neuron to the dynamics of the Aplysia feeding network. J Neurophysiol 97:3046-3056.
44. Proekt A, Vilim FS, Alexeeva V, Brezina V, Friedman A, Jing J, Li L, Zhurov Y, Sweedler JV, Weiss KR (2005) Identification of a new neuropeptide precursor reveals a novel source of extrinsic modulation in the feeding system of Aplysia. J Neurosci 25:9637-9648.
45. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G (2006) Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9:1526-1533.
46. Roberts PD, Bell CC (2002) Active control of spike-timing dependent synaptic plasticity in an electrosensory system. J Physiol (Paris) 96:445-449.
47. 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.
48. Saideman SR, Blitz DM, Nusbaum MP (2007) Convergent motor patterns from divergent circuits. J Neurosci 27:6664-6674.
49. Sakurai A, Darghouth NR, Butera RJ, Katz PS (2006) Serotonergic enhancement of a 4-AP-sensitive current mediates the synaptic depression phase of spike timing-dependent neuromodulation. J Neurosci 26:2010-2021.
50. Sanchez JA, Kirk MD (2000) Short-term synaptic enhancement modulates ingestion motor programs of Aplysia. J Neurosci 20:RC 85:1-7.
51. Sasaki K, Due MR, Jing J, Weiss KR (2007) The feeding CPG in Aplysia directly controls two distinct outputs of a compartmentalized interneuron that functions as a CPG element. J Neurophysiol 98:3796-3801.
52. Shaw BK, Kristan WB (1997) The neuronal basis of the behavioral choice between swimming and shortening in the leech: control is not selectively exercised at higher circuit levels. J Neurosci 17:786-795.
53. Soffe SR (1993) Two distinct rhythmic motor patterns are driven by common premotor and motor neurons in a simple vertebrate spinal cord. J Neurosci 13:4456-4469.
54. Thirumalai V, Prinz AA, Johnson CD, Marder E (2006) Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period. J Neurophysiol 95:1762-1770.
55. Wu JS, Due MR, Sasaki K, Proekt A, Jing J, Weiss KR (2007) State dependence of spike timing and neuronal function in a motor pattern generating network. J Neurosci 27:10818-10831.
56. Zelenin PV, Grillner S, Orlovsky GN, Deliagina TG (2001) Heterogeneity of the population of command neurons in the lamprey. J Neurosci 21:7793-7803.
57. Zhurov Y, Proekt A, Weiss KR, Brezina V (2005) Changes of internal state are expressed in coherent shifts of neuromuscular activity in Aplysia feeding behavior. J Neurosci 25:1268-1280.