Cycle-to-cycle variability of neuromuscular activity in Aplysia feeding behavior

Journal of Neurophysiology

Volumn 92, Issue 1, 2004, Pages 157-180

  Horn, Charles C ^a,b   Zhurov, Yuriy ^c   Orekhova, Irina V ^c   Proekt, Alex ^c   Kupfermann, Irving ^b   Weiss, Klaudiusz R ^c   Brezina, Vladimir ^c  

^a MONELL CHEMICAL SENSES CENTER   (United States)

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

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCESSORY RADULA CLOSER MUSCLE; ANIMAL BEHAVIOR; ANIMAL TISSUE; APLYSIA; ARTICLE; BITE; CONTROLLED STUDY; ELECTRODE; ESOPHAGEAL NERVE; ESOPHAGUS; FEEDING BEHAVIOR; MOTONEURON; MUSCLE CONTRACTION; NEUROMUSCULAR FUNCTION; NEUROMUSCULAR SYSTEM; NONHUMAN; PRIORITY JOURNAL; RADULA OPENER MUSCLE; SEAWEED; STEREOTYPY; SWALLOWING; TONGUE;

ACTION POTENTIALS; ANIMALS; APLYSIA; ELECTRIC STIMULATION; FEEDING BEHAVIOR; GANGLIA, INVERTEBRATE; MUSCLE CONTRACTION; NEUROMUSCULAR JUNCTION;

EID: 1842449059     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01190.2003     Document Type: Article

References (68)

1. Beer RD, Chiel HJ, and Gallagher JC. Evolution and analysis of model CPGs for walking. II. General principles and individual variability. J Comput Neurosci 7: 119-147, 1999.
2. Bernstein N. The Co-ordination and Regulation of Movement. Oxford, UK: Pergamon Press, 1967.
3. Brezina V, Orekhova IV, and Weiss KR. Functional uncoupling of linked neurotransmitter effects by combinatorial convergence. Science 273: 806-810, 1996.
4. Brezina V, Orekhova IV, and Weiss KR. Control of time-dependent biological processes by temporally patterned input. Proc Natl Acad Sci USA 94: 10444-10449, 1997.
5. Brezina V, Orekhova IV, and Weiss KR. The neuromuscular transform: the dynamic, nonlinear link between motor neuron firing patterns and muscle contraction in rhythmic behaviors. J Neurophysiol 83: 207-231, 2000a.
6. Brezina V, Orekhova IV, and Weiss KR. Optimization of rhythmic behaviors by modulation of the neuromuscular transform. J Neurophysiol 83: 260-279, 2000b.
7. Brezina V, Orekhova IV, and Weiss KR. Neuromuscular modulation in Aplysia. I. Dynamic model. J Neurophysiol 90: 2592-2612, 2003a.
8. Brezina V, Orekhova IV, and Weiss KR. Neuromuscular modulation in Aplysia. II. Modulation of the neuromuscular transform in behavior. J Neurophysiol 90: 2613-2628, 2003b.
9. Brezina V and Weiss KR. The neuromuscular transform constrains the production of functional rhythmic behaviors. J Neurophysiol 83: 232-259, 2000.
10. Chase R. Behavior and Its Neural Control in Gastropod Molluscs. Oxford, UK: Oxford Univ. Press, 2002.
11. Chiel HJ and Beer RD. The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci 20: 553-557, 1997.
12. Chiel HJ, Weiss KR, and Kupfermann I. An identified histaminergic neuron modulates feeding motor circuitry in Aplysia. J Neurosci 6: 2427-2450, 1986.
13. Church PJ and Lloyd PE. Activity of multiple identified motor neurons recorded intracellularly during evoked feedinglike motor programs in Aplysia. J Neurophysiol 72: 1794-1809, 1994.
14. Cohen JL, Weiss KR, and Kupfermann I. Motor control of buccal muscles in Aplysia. J Neurophysiol 41: 157-180, 1978.
15. Croll RP, Davis WJ, and Kovac MP. Neural mechanisms of motor program switching in the mollusc Pleurobranchaea. I. Central motor programs underlying ingestion, egestion, and the "neutral" rhythm(s). J Neurosci 5: 48-55, 1984.
16. Cropper EC, Kupfermann I, and Weiss KR. Differential firing patterns of the peptide-containing cholinergic motor neurons B15 and B16 during feeding behavior in Aplysia. Brain Res 522: 176-179, 1990.
17. de Ruyter van Steveninck RR, Lewen GD, Strong SP, Koberle R, and Bialek W. Reproducibility and variability in neural spike trains. Science 275: 1805-1808, 1997.
18. Drushel RF, Neustadter DM, Hurwitz I, Crago PE, and Chiel HJ. Kinematic models of the buccal mass of Aplysia californica. J Exp Biol 201: 1563-1583, 1998.
19. Drushel RF, Neustadter DM, Shallenberger LL, Crago PE, and Chiel HJ. The kinematics of swallowing in the buccal mass of Aplysia californica. J Exp Biol 200: 735-752, 1997.
20. Elliott CJH and Susswein AJ. Comparative neuroethology of feeding control in molluscs. J Exp Biol 205: 877-896, 2002.
21. Elson RC, Huerta R, Abarbanel HDI, Rabinovich MI, and Selverston AI. Dynamic control of irregular bursting in an identified neuron of an oscillatory circuit. J Neurophysiol 82: 115-122, 1999.
22. Evans CG, Rosen S, Kupfermann I, Weiss KR, and Cropper EC. Characterization of a radula opener neuromuscular system in Aplysia. J Neurophysiol 76: 1267-1281, 1996.
23. Hand D, Mannila H, and Smyth P. Principles of Data Mining. Cambridge, MA: MIT Press, 2001.
24. Hoel PG. Introduction to Mathematical Statistics (4th ed.). New York: Wiley, 1971.
25. Hooper SL, Brezina V, Cropper EC, and Weiss KR. Flexibility of muscle control by modulation of muscle properties. In: Beyond Neurotransmission: Neuromodulation and Its Importance for Information Processing, edited by Katz PS. Oxford, UK: Oxford Univ. Press, 1999, p. 241-274.
26. Hoover NJ, Weaver AL, Harness PI, and Hooper SL. Combinatorial and cross-fiber averaging transform muscle electrical responses with a large stochastic component into deterministic contractions. J Neurosci 22: 1895-1904, 2002.
27. Horn CC, Benjamin PR, Weiss KR, and Kupfermann I. Decrement of the response of a serotonergic modulatory neuron (the metacerebral cell) in Aplysia, during repeated presentation of appetitive (food) stimuli. Neurosci Lett 267: 161-164, 1999.
28. Horn CC and Kupfermann I. Egestive feeding responses in Aplysia persist after sectioning of the cerebral-buccal connectives: evidence for multiple sites of control of motor programs. Neurosci Lett 323: 175-178, 2002.
29. Hurwitz I, Goldstein RS, and Susswein AJ. 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, 1994.
30. Hurwitz I, Neustadter D, Morton DW, Chiel HJ, and Susswein AJ. 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, 1996.
31. Hurwitz I and Susswein AJ. Adaptation of feeding sequences in Aplysia oculifera to changes in the load and width of food. J Exp Biol 166: 215-235, 1992.
32. Jing J and Weiss KR. Neural mechanisms of motor program switching in Aplysia. J Neurosci 21: 7349-7362, 2001.
33. Kabotyanski EA, Baxter DA, Cushman SJ, and Byrne JH. Modulation of fictive feeding by dopamine and serotonin in Aplysia. J Neurophysiol 83: 374-392, 2000.
34. Kara P, Reinagel P, and Reid RC. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27: 635-646, 2000.
35. Kupfermann I. Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol 10: 1-26, 1974.
36. Kupfermann I, Brezina V, Cropper EC, Deodhar D, Probst WC, Rosen SC, Vilim FS, and Weiss KR. Reconfiguration of the peripheral plant during various forms of feeding behaviors in the mollusc Aplysia. In: Neurons, Networks, and Motor Behavior, edited by Stein PSG, Grillner S, Selverston AI, and Stuart DG. Cambridge, MA: MIT Press, 1997, p. 217-222.
37. Morgan PT, Jing J, Vilim FS, and Weiss KR. Interneuronal and peptidergic control of motor pattern switching in Aplysia. J Neurophysiol 87: 49-61, 2002.
38. Morton DW and Chiel HJ. In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia. J Comp Physiol A Sens Neural Behav Physiol 172: 17-32, 1993a.
39. Morton DW and Chiel HJ. The timing of activity in motor neurons that produce radula movements distinguishes ingestion from rejection in Aplysia. J Comp Physiol A Sens Neural Behav Physiol 173: 519-536, 1993b.
40. Mpitsos GJ. Attractors: architects of network organization? Brain Behav Evol 55: 256-277, 2000.
41. Nargeot R, Baxter DA, and Byrne JH. Contingent-dependent enhancement of rhythmic motor patterns: an in vitro analog of operant conditioning. J Neurosci 17: 8093-8105, 1997.
42. Nargeot R, Baxter DA, and Byrne JH. In vitro analog of operant conditioning in Aplysia. I. Contingent reinforcement modifies the functional dynamics of an identified neuron. J Neurosci 19: 2247-2260, 1999a.
43. Nargeot R, Baxter DA, and Byrne JH. In vitro analog of operant conditioning in Aplysia. II. Modifications of the functional dynamics of an identified neuron contribute to motor pattern selection. J Neurosci 19: 2261-2272, 1999b.
44. Neustadter DM, Drushel RF, and Chiel HJ. Kinematics of the buccal mass during swallowing based on magnetic resonance imaging in intact, behaving Aplysia californica. J Exp Biol 205: 939-958, 2002a.
45. Neustadter DM, Drushel RF, Crago PE, Adams BW, and Chiel HJ. A kinematic model of swallowing in Aplysia californica based on radula/odontophore kinematics and in vivo magnetic resonance images. J Exp Biol 205: 3177-3206, 2002b.
46. Orekhova IV, Alexeeva V, Church PJ, Weiss KR, and Brezina V. Multiple presynaptic and postsynaptic sites of inhibitory modulation by myomodulin at ARC neuromuscular junctions of Aplysia. J Neurophysiol 89: 1488-1502, 2003.
47. Orekhova IV, Jing J, Brezina V, DiCaprio RA, Weiss KR, and Cropper EC. Sonometric measurements of motor-neuron evoked movements of an internal feeding structure (the radula) in Aplysia. J Neurophysiol 86: 1057-1061, 2001.
48. Press WH, Teukolsky SA, Vetterling WT, and Flannery BP. Numerical Recipes in C++: The Art of Scientific Computing (2nd ed.). Cambridge, UK: Cambridge Univ. Press, 2002.
49. Proekt A and Weiss KR. Intrinsic and extrinsic sources of plasticity contribute to the formation of persistent behavioral states in the feeding circuitry of Aplysia. Abstract 67.23, 2002 Abstract Viewer. Washington, DC: Society for Neuroscience. Online, 2002.
50. Proekt A and Weiss KR. Convergent mechanisms mediate preparatory states and repetition priming in the feeding network of Aplysia. J Neurosci 23: 4029-4033, 2003.
51. Rabinovich MI and Abarbanel HDI. The role of chaos in neural systems. Neuroscience 87: 5-14, 1998.
52. Scholz JP and Schöner G. The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126: 289-306, 1999.
53. Schöner G and Kelso JAS. Dynamic pattern generation in behavioral and neural systems. Science 239: 1513-1520, 1988.
54. Selverston AI, Rabinovich MI, Abarbanel HDI, Elson R, Szücs A, Pinto RD, Huerta R, and Varona P. Reliable circuits from irregular neurons: a dynamical approach to understanding central pattern generators. J Physiol (Paris) 94: 357-374, 2000.
55. Shadlen MN and Newsome WT. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18: 3870-3896, 1998.
56. Sparks DL, Kristan WB, and Shaw BK. The role of population coding in the control of movement. In: Neurons, Networks, and Motor Behavior, edited by Stein PSG, Grillner S, Selverston AI, and Stuart DG. Cambridge, MA: MIT Press, 1997, p. 21-32.
57. Stein PSG, Grillner S, Selverston AI, and Stuart DG. Neurons, Networks, and Motor Behavior. Cambridge, MA: MIT Press, 1997.
58. Stevens CF and Zador AM. Input synchrony and the irregular firing of cortical neurons. Nat Neurosci 1: 210-217, 1998.
59. Susswein AJ, Kupfermann I, and Weiss KR. The stimulus control of biting in Aplysia. J Comp Physiol 108: 75-96, 1976.
60. Susswein AJ, Schwarz M, and Feldman E. Learned changes of feeding behavior in Aplysia in response to edible and inedible foods. J Neurosci 6: 1513-1527, 1986.
61. Todorov E and Jordan MI. Optimal feedback control as a theory of motor coordination. Nat Neurosci 5: 1226-1235, 2002.
62. von Neumann J. Probabilistic logics and the synthesis of reliable organisms from unreliable components. In: Automata Studies, edited by Shannon CE and McCarthy J. Princeton, NJ: Princeton Univ. Press, 1956, p. 43-98.
63. Warzecha A-K and Egelhaaf M. Variability in spike trains during constant and dynamic stimulation. Science 283: 1927-1930, 1999.
64. Weiss KR, Chiel HJ, Koch U, and Kupfermann I. Activity of an identified histaminergic neuron, and its possible role in arousal of feeding behavior in semi-intact Aplysia. J Neurosci 6: 2403-2415, 1986.
65. Weiss KR, Mandelbaum DE, Schonberg M, and Kupfermann I. Modulation of buccal muscle contractility by serotonergic metacerebral cells in Aplysia: evidence for a role of cyclic adenosine monophosphate. J Neurophysiol 42: 791-803, 1979.
66. Wu J-Y, Tsau Y, Hopp H-P, Cohen LB, Tang AC, and Falk CX. Consistency in nervous systems: trial-to-trial and animal-to-animal variations in the responses to repeated applications of a sensory stimulus in Aplysia. J Neurosci 14: 1366-1384, 1994.
67. Zhurov Y, Proekt A, Weiss KR, and Brezina V. History-dependent changes in the character of feeding motor programs in Aplysia are accompanied by changes in the character of muscle contractions. Abstract 500.13, 2003 Abstract Viewer. Washington, DC: Society for Neuroscience. Online, 2003.
68. Zoccolan D, Pinato G, and Torre V. Highly variable spike trains underlie reproducible sensorimotor responses in the medicinal leech. J Neurosci 22: 10790-10800, 2002.