Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 192, Issue 8, 2006, Pages 857-870

  Novakovic, Valerie A ^a,d   Sutton, Gregory P ^b   Neustadter, David M ^c,e   Beer, Randall D ^a,b   Chiel, Hillel J ^a,c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Case Western Reserve University   (United States)

^c Case Western Reserve University   (United States)

^d VA BOSTON HEALTHCARE SYSTEM   (United States)

^e NONE   (Israel)

Author keywords

Biomechanics; Feeding; Mollusk; Muscular hydrostat; Soft tissue

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; APLYSIA; ARTICLE; BIOMECHANICS; COMPARATIVE STUDY; ELECTROMYOGRAPHY; FEEDING BEHAVIOR; HISTOLOGY; INNERVATION; JAW; METHODOLOGY; MOUTH; MUSCLE; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; SWALLOWING;

ANIMALS; APLYSIA; BEHAVIOR, ANIMAL; BIOMECHANICS; DEGLUTITION; ELECTROMYOGRAPHY; FEEDING BEHAVIOR; JAW; MAGNETIC RESONANCE IMAGING; MOUTH; MUSCLES;

EID: 33746434444     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-006-0124-7     Document Type: Article

References (57)

1. Ahn AN, Full RJ (2002) A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect. J Exp Biol 205:379-389
2. Brezina V, Orekhova IV, Weiss KR (1996) Functional uncoupling of linked neurotransmitter effects by combinatorial convergence. Science 273:806-810
3. Brezina V, Orekhova IV, Weiss KR (2000a) The neuromuscular transform: the dynamic, nonlinear link between motor neuron firing patterns and muscle contraction in rhythmic behaviors. J Neurophysiol 83:207-231
4. Brezina V, Orehova IV, Weiss KR (2000b) Optimization of rhythmic behaviors by modulation of the neuromuscular transform. J Neurophysiol 83:260-279
5. Brezina V, Orekhova IV, Weiss KR (2003) Neuromuscular modulation in Aplysia. II. Modulation of the neuromuscular transform in behavior. J Neurophysiol 90:2613-2628
6. Brezina V, Horn CC, Weiss KR (2005) Modeling neuromuscular modulation in Aplysia. III. Interaction of central motor commands and peripheral modulatory state for optimal behavior. J Neurophysiol 93:1523-1556
7. Brusca RC, Brusca GJ (1990) Invertebrates. Sinauer Associates, Sunderland
8. Chiel HJ, Beer RD (1997) The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci 20:553-557
9. Chiel HJ, Crago P, Mansour JM, Hathi K (1992) Biomechanics of a muscular hydrostat: a model of lapping by a reptilian tongue. Biol Cybern 67:403-415
10. Church PJ, Cohen KP, Scott ML, Kirk MD (1991) Peptidergic motoneurons in the buccal ganglia of Aplysia californica: immunocytochemical, morphological, and physiological characterizations. J Comp Physiol A 168:323-336
11. Dickinson MH, Farley CT, Full RJ, Koehl MA, Kram R, Lehman S (2000) How animals move: An integrative view. Science 288:100-106
12. Drushel RF, Neustadter DM, Shallenberger LL, Crago PE, Chiel HJ (1997) The kinematics of swallowing in the buccal mass of Aplysia californica. J Exp Biol 200:735-752
13. Drushel RF, Neustadter DM, Hurwitz I, Crago PE, Chiel HJ (1998) Kinematic models of the buccal mass of Aplysia californica. J Exp Biol 201:1563-1583
14. Drushel RF, Sutton GP, Neustadter DM, Mangan EV, Adams BW, Crago PE, Chiel HJ (2002) Radula-centric and odontophore-centric kinematic models of swallowing in Aplysia californica. J Exp Biol 205:2029-2051
15. Evans CG, Cropper EC (1998) Proprioceptive input to feeding motor programs in Aplysia. J Neurosci 18:8016-8031
16. Evans CG, Alexeeva V, Rybak J, Karhunen T, Weiss KR, Cropper EC (1999) A pair of reciprocally inhibitory histaminergic sensory neurons are activated within the same phase of ingestive motor programs in Aplysia. J Neurosci 19:845-858
17. Fox LE, Lloyd PE (1997) Serotonin and the small cardioactive peptides differentially modulate two motor neurons that innervate the same muscle fibers in Aplysia. J Neurosci 17:6064-6074
18. Fox LE, Lloyd PE (1998) Serotonergic neurons differentially modulate the efficacy of two motor neurons innervating the same muscle fibers in Aplysia. J Neurophysiol 80:647-655
19. Howells HH (1942) The structure and function of the alimentary canal of Aplysia punctata. Q J Microsc Sci 83:357-397
20. Hurwitz I, Susswein AJ (1992) Adaptation of feeding sequences in Aplysia oculifera to changes in the load and width of food. J Exp Biol 166:215-235
21. Hurwitz I, Neustadter DM, 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. Hurwitz I, Cropper EC, Vilim FS, Alexeeva V, Susswein AJ, Kupfermann I, Weiss KR (2000) Serotonergic and peptidergic modulation of the buccal mass protractor muscle (I2) in Aplysia. J Neurophysiol 84:2810-2820
23. Katz PS, Frost WN (1996) Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19:54-61
24. Kier WM, van Leeuwen JL (1997) A kinematic analysis of tentacle extension in the squid Loligo pealei. J Exp Biol 200:41-53
25. Kier WM, Smith KK (1985) Tongues, tentacles and trunks: the biomechanics of movement in muscular-hydrostats. Zool J Linnean Soc 83:307-324
26. Kupfermann I (1974) Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol 10:1-26
27. LeBeau FE, El Manira A, Grillner S (2005) Tuning the network: modulation of neuronal microcircuits in the spinal cord and hippocampus. Trends Neurosci 28:552-561
28. Mallett ES, Yamaguchi GT, Birch JM, Nishikawa KC (2001) Feeding motor patterns in anurans: Insights from biomechanical modeling. Am Zool 41:1364-1374
29. Messenger JB, Young JZ (1999) The radular apparatus of cephalopods. Phil Trans R Soc Lond B 354:161-182
30. Moon BR (2000) The mechanics of swallowing and the muscular control of diverse behaviours in gopher snakes. J Exp Biol 203:2589-2601
31. 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
32. 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
33. Nagahama, Shin (1998) Patterned jaw movements and the motor neuron activity during rejection of seaweed in Aplysia kurodai. J Comp Physiol A (1998) 182:551-562
34. Nagahama T, Takata M (1988) Food-induced firing patterns in motoneurons producing jaw movements in Aplysia kurodai. J Comp Physiol A 162:729-738
35. Neustadter DM, Chiel HJ (2004) Imaging freely moving subjects using continuous interleaved orthogonal magnetic resonance imaging. Magn Reson Imaging 22:329-343
36. Neustadter DM, Drushel RF, Chiel HJ (2002a) Kinematics of the buccal mass during swallowing based on magnetic resonance imaging in intact, behaving Aplysia californica. J Exp Biol 205:939-958
37. Neustadter DM, Drushel RF, Crago PE, Adams BW, Chiel HJ (2002b) 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
38. Nishikawa KC (1999) Neuromuscular control of prey capture in frogs. Phil Trans R Soc Lond B 354:941-954
39. Ritzmann RE (1974) Mechanisms for the snapping behavior of two alpheid shrimp, Alpheus californiensis and Alpheus heterochelis. J Comp Physiol A 95:217-236
40. Rose RM (1971) Functional morphology of the buccal mass of the nudibranch Archidoris pseudoargus. J Zool Lond 165:317-336
41. Rose RM, Benjamin PR (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol 80:137-163
42. Rosen SC, Miller MW, Cropper EC, Kupfermann I (2000a) Outputs of radula mechanoafferent neurons in Aplysia are modulated by motor neurons, interneurons and sensory neurons. J Neurophysiol 83:1621-1636
43. Rosen SC, Miller MW, Evans CG, Cropper EC, Kupfermann I (2000b) Diverse synaptic connections between peptidergic radula mechanoafferent neurons and neurons in the feeding system of Aplysia. J Neurophysiol 83:1605-1620
44. Scheepens WA, Jongen MM, Nieman FH, de Bie RA, Weil EH, van Kerrebroeck PE (2002) Predictive factors for sacral neuromodulation in chronic lower urinary tract dysfunction. Urology 60:598-602
45. Scott ML, Govind CK, Kirk MD (1991) Neuromuscular organization of the buccal system in Aplysia californica. J Comp Neurol 312:207-222
46. Smith DA (1988) Radular kinetics during grazing in Helisoma trivolvis (Gastropoda: pulmonata). J Exp Biol 136:89-102
47. Sutton GP, Macknin JB, Gartman SS, Sunny GP, Beer RD, Crago PE, Neustadter DM, Chiel HJ (2004a) Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing. J Comp Physiol A 190:501-514
48. Sutton GP, Mangan EV, Neustadter DM, Beer RD, Crago PE, Chiel HJ (2004b) Neural control exploits changing mechanical advantage and context dependence to generate different feeding responses in Aplysia. Biol Cybern 91:333-345
49. Uyeno TA, Kier WM (2005) Functional morphology of the cephalopod buccal mass: a novel joint type. J Morphol 264:211-222
50. Van Leeuwen JL (1991) Optimum power output and structural design of sarcomeres. J Theor Biol 149:229-256
51. Van Leeuwen JL, Kier WM (1997) Functional design of tentacles in squid: Linking sarcomere ultrastructure to gross morphological dynamics. Phil Trans R Soc Lond B 352:551-571
52. Wilson JF, Mahajan U, Wainwright SA, Croner LJ (1991) A continuum model of elephant trunks. J Biomech Eng 113:79-84
53. Wine JJ, Krasne FB (1982) The cellular organization of the crayfish escape behavior. In: Sandeman DC, Atwood HL (eds) The Biology of Crustacea, Chapter 4. Academic, New York, pp 241-492
54. Ye H, Morton DW, Chiel HJ (2006) Neuromechanics of coordination during swallowing in Aplysia californica. J Neurosci 26:1470-1485
55. Yu S-N, Crago PE, Chiel HJ (1999) Biomechanical properties and a kinetic simulation model of the smooth muscle I2 in the buccal mass of Aplysia. Biol Cybern 81:505-513
56. Zajac FE (1989) Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng 17:359-411
57. Zajac FE (1993) Muscle coordination of movement: a perspective. J Biomech 26(Suppl 1):109-124