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Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica

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Abstract

Muscular hydrostats, such as tongues, trunks or tentacles, have fewer constraints on their degrees of freedom than musculoskeletal systems, so changes in a structure’s shape may alter the positions and lengths of other components (i.e., induce mechanical reconfiguration). We studied mechanical reconfiguration during rejection and swallowing in the marine mollusk Aplysia californica. During rejection, inedible material is pushed out of an animal’s buccal cavity. The grasper (radula/odontophore) closes on inedible material, and then a posterior muscle, I2, pushes the grasper toward the jaws (protracts it). After the material is released, an anterior muscle complex (the I1/I3/jaw complex) pushes the grasper toward the esophagus (retracts it). During swallowing, the grasper is protracted open, and then retracts closed, pulling in food. Grasper closure changes its shape. Magnetic resonance images show that grasper closure lengthens I2. A kinetic model quantified the changes in the ability of I2 and I1/I3 to exert force as grasper shape changed. Grasper closure increases I2’s ability to protract during rejection, and increases I1/I3’s ability to retract during swallowing. Motor neurons controlling radular closure may therefore affect the behavioral outputs of I2’s and I1/I3’s motor neurons. Thus, motor neurons may modulate the outputs of other motor neurons through mechanical reconfiguration.

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Abbreviations

I2:

Intrinsic buccal muscle 2

I1/I3:

Intrinsic buccal muscles 1 and 3

LT:

Length/tension

FI2:

Force in I2

Fmax:

Maximum force

BML:

Buccal mass lengths

B8a,b, B61, B62, B63:

Buccal ganglion motor neurons and interneurons

References

  • 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

    PubMed  CAS  Google Scholar 

  • Brezina V, Orekhova IV, Weiss KR (1996) Functional uncoupling of linked neurotransmitter effects by combinatorial convergence. Science 273:806–810

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Brezina V, Orehova IV, Weiss KR (2000b) Optimization of rhythmic behaviors by modulation of the neuromuscular transform. J Neurophysiol 83:260–279

    CAS  Google Scholar 

  • Brezina V, Orekhova IV, Weiss KR (2003) Neuromuscular modulation in Aplysia. II. Modulation of the neuromuscular transform in behavior. J Neurophysiol 90:2613–2628

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Brusca RC, Brusca GJ (1990) Invertebrates. Sinauer Associates, Sunderland

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dickinson MH, Farley CT, Full RJ, Koehl MA, Kram R, Lehman S (2000) How animals move: An integrative view. Science 288:100–106

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Evans CG, Cropper EC (1998) Proprioceptive input to feeding motor programs in Aplysia. J Neurosci 18:8016–8031

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Howells HH (1942) The structure and function of the alimentary canal of Aplysia punctata. Q J Microsc Sci 83:357–397

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Katz PS, Frost WN (1996) Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19:54–61

    Article  PubMed  CAS  Google Scholar 

  • Kier WM, van Leeuwen JL (1997) A kinematic analysis of tentacle extension in the squid Loligo pealei. J Exp Biol 200:41–53

    PubMed  Google Scholar 

  • Kier WM, Smith KK (1985) Tongues, tentacles and trunks: the biomechanics of movement in muscular-hydrostats. Zool J Linnean Soc 83:307–324

    Article  Google Scholar 

  • Kupfermann I (1974) Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol 10:1–26

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mallett ES, Yamaguchi GT, Birch JM, Nishikawa KC (2001) Feeding motor patterns in anurans: Insights from biomechanical modeling. Am Zool 41:1364–1374

    Article  Google Scholar 

  • Messenger JB, Young JZ (1999) The radular apparatus of cephalopods. Phil Trans R Soc Lond B 354:161–182

    Article  Google Scholar 

  • Moon BR (2000) The mechanics of swallowing and the muscular control of diverse behaviours in gopher snakes. J Exp Biol 203:2589–2601

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nagahama T, Takata M (1988) Food-induced firing patterns in motoneurons producing jaw movements in Aplysia kurodai. J Comp Physiol A 162:729–738

    Article  Google Scholar 

  • Neustadter DM, Chiel HJ (2004) Imaging freely moving subjects using continuous interleaved orthogonal magnetic resonance imaging. Magn Reson Imaging 22:329–343

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Nishikawa KC (1999) Neuromuscular control of prey capture in frogs. Phil Trans R Soc Lond B 354:941–954

    Article  CAS  Google Scholar 

  • Ritzmann RE (1974) Mechanisms for the snapping behavior of two alpheid shrimp, Alpheus californiensis and Alpheus heterochelis. J Comp Physiol A 95:217–236

    Article  Google Scholar 

  • Rose RM (1971) Functional morphology of the buccal mass of the nudibranch Archidoris pseudoargus. J Zool Lond 165:317–336

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Scott ML, Govind CK, Kirk MD (1991) Neuromuscular organization of the buccal system in Aplysia californica. J Comp Neurol 312:207–222

    Article  PubMed  CAS  Google Scholar 

  • Smith DA (1988) Radular kinetics during grazing in Helisoma trivolvis (Gastropoda: pulmonata). J Exp Biol 136:89–102

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Uyeno TA, Kier WM (2005) Functional morphology of the cephalopod buccal mass: a novel joint type. J Morphol 264:211–222

    Article  PubMed  Google Scholar 

  • Van Leeuwen JL (1991) Optimum power output and structural design of sarcomeres. J Theor Biol 149:229–256

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wilson JF, Mahajan U, Wainwright SA, Croner LJ (1991) A continuum model of elephant trunks. J Biomech Eng 113:79–84

    Article  PubMed  CAS  Google Scholar 

  • 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

  • Ye H, Morton DW, Chiel HJ (2006) Neuromechanics of coordination during swallowing in Aplysia californica. J Neurosci 26:1470–1485

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zajac FE (1989) Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng 17:359–411

    PubMed  CAS  Google Scholar 

  • Zajac FE (1993) Muscle coordination of movement: a perspective. J Biomech 26(Suppl 1):109–124

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the NSF (IBN-0218386 to HJC) and the NIH (NS-047073 to HJC), and the NSF IGERT program (Grant 345–1898) for their support of this research. We also thank Richard Drushel for the illustration of the buccal mass anatomy (Fig. 1a), and for his helpful comments on the research in this paper, and Robert Herman for his sketches of the MRI. Experiments described in this study comply with the Principles of animal care, publication No. 86-23, revised 1985, of the National Institute of Health, and also with the current laws of the United States.

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Author notes

  1. Valerie A. Novakovic

    Present address: Veterans Administration Boston Healthcare System, 1400 VFW Parkway Building 3, Room 2A110, West Roxbury, MA, 02132, USA

  2. David M. Neustadter

    Present address: , Ruth Hamoavia 3, Apt. 3, Netanya, 42756, Israel

Authors and Affiliations

  1. Department of Biology, Case Western Reserve University, 2080 Adelbert Road, Cleveland, OH, 44106, USA

    Valerie A. Novakovic, Randall D. Beer & Hillel J. Chiel

  2. Department of Mechanical and Aerospace Engineering, Case Western Reserve University, 10900 Euclid Avenue, 44106-7222, Cleveland, OH, USA

    Gregory P. Sutton

  3. Department of Biomedical Engineering, Case Western Reserve University, 319 Wickendon Building, 10900 Euclid Avenue, 44106-7207, Cleveland, OH, USA

    David M. Neustadter & Hillel J. Chiel

  4. Department of Electrical Engineering and Computer Science, Case Western Reserve University, 10900 Euclid Avenue, 44106-7071, Cleveland, OH, USA

    Randall D. Beer

  5. Department of Neurosciences School of Medicine, Case Western Reserve University, 2109 Adelbert Road, 44106-4975, Cleveland, OH, USA

    Hillel J. Chiel

Authors
  1. Valerie A. Novakovic
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Corresponding author

Correspondence to Hillel J. Chiel.

Additional information

Valerie A. Novakovic and Gregory P. Sutton contributed equally to the paper.

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Novakovic, V.A., Sutton, G.P., Neustadter, D.M. et al. Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica . J Comp Physiol A 192, 857–870 (2006). https://doi.org/10.1007/s00359-006-0124-7

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  • DOI: https://doi.org/10.1007/s00359-006-0124-7

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