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Investigating localized sensitivity in the feeding patterns of Aplysia californica

Kendrick M. Shaw1*, Miranda J. Cullins1, Hui Lu1, Jeffrey M. McManus1, Peter J. Thomas2 and Hillel J. Chiel3
  • 1 Case Western Reserve University, Biology, United States
  • 2 Case Western Reserve University, Mathematics, Biology, Cognitive Science, United States
  • 3 Case Western Reserve University, Biology, Neuroscience, Biomedical Engineering, United States

Many behaviors such as breathing, walking, and swallowing require the nervous system to generate stereotyped sequences of motor activation. These sequences often display significant timing changes in specific components, even though much of the pattern is unchanged, as an animal performs a behavior. For example, in cat walking, the stance phase is shortened much more than the swing phase as the animal walks more quickly (Halbertsma, 1983). Changes in sensory feedback appear to be sufficient to cause these changes in timing (Grillner, 1981), and the strength of the relevant reflexes are modulated by the phase of the cycle (Akazawa, 1982, Stein 2000), suggesting a potential role for phase dependent changes in the sensitivity of phase duration to sensory input. These adjustments in timing may be critical for for adapting the behavior to the changing environmental demands that an animal faces.

During these phases with variable timing, the output of the nervous system may change very slowly, as if the nervous system is dwelling in a localized part of the pattern for a variable amount of time before moving on to the next phase of the behavior. We hypothesize that within these regions, the effect of the intrinsic neural activity driving progression through the pattern becomes small relative to the effects of sensory input and noise on progression through the pattern. In particular, we predict that the passage through these regions can be well modeled by a trajectory passing near a saddle equilibrium point (e.g. Spardy 2011), i.e., a point that attracts trajectories along some directions and repels them along others, rather than traveling along a more typical trajectory with more uniform flow.

To explore this hypothesis, we are investigating the control of protraction and retraction of the radula/odontophore during feeding in the marine mollusk Aplysia californica. Most of the variability in timing of these behaviors appears in specific parts of the motor pattern. In addition, the distribution of the times spent in these portions of the patterns is significantly skewed (i.e. has a heavy tail), rather than the more Gaussian distribution expected when the contribution of noise is small relative to the drift.

If the hypothesis is true, we also expect the effects of small perturbations on the duration of that part of the motor pattern to be much greater for perturbations made when the system is first entering that portion of the pattern than an identical perturbation made later during that portion of the pattern (Shaw, 2012). To investigate this, we are attempting to briefly stimulate a retraction phase neuron, B64 (Hurwitz, 1996), during I2 activity (a proxy for protraction in vitro) in an isolated buccal ganglion, and similarly stimulate the neuron B52 (Plummer, 1990) (hypothesized to terminate retraction, (Nargeot, 2002)) during the retraction phase of an in vitro pattern.

These studies may help to illuminate the underlying dynamics of the feeding pattern generator in Aplysia, and may also serve to provide insights into the dynamical properties of other pattern generators in vertebrates and humans.

References

Akazawa, K., Aldridge, J. W., Steeves, J. D., & Stein, R. B. (1982). Modulation of Stretch Reflexes During Locomotion in the Mesencephalic Cat. The Journal of Physiology, 329(1), 553–567.

Grillner, S. (1981). "Control of Locomotion in Bipeds, Tetrapods, and Fish." in Comprehensive Physiology, ed R. Terjung (Hoboken, NJ, USA: John Wiley & Sons, Inc.)

Halbertsma, J. M. (1983). The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. Acta physiologica Scandinavica. Supplementum, 521, 1–75.

Hurwitz, I., & Susswein, A. J. (1996). B64, a newly identified central pattern generator element producing a phase switch from protraction to retraction in buccal motor programs of Aplysia californica. Journal of Neurophysiology, 75(4), 1327 –1344.

Nargeot, R., Baxter, D. A., & Byrne, J. H. (2002). Correlation between activity in neuron B52 and two features of fictive feeding in Aplysia. Neuroscience Letters, 328(2), 85–88. doi:10.1016/S0304-3940(02)00468-8

Plummer, M. R., & Kirk, M. D. (1990). Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: synaptic connections, effects on ongoing motor rhythms, and peptide modulation. Journal of Neurophysiology, 63(3), 539 –558.

Shaw, K. M., Park, Y.-M., Chiel, H. J., & Thomas, P. J. (2012). Phase Resetting in an Asymptotically Phaseless System: On the Phase Response of Limit Cycles Verging on a Heteroclinic Orbit. SIAM Journal on Applied Dynamical Systems, 11, 350–391. doi:10.1137/110828976

Spardy, L. E., Markin, S. N., Shevtsova, N. A., Prilutsky, B. I., Rybak, I. A., & Rubin, J. E. (2011). A dynamical systems analysis of afferent control in a neuromechanical model of locomotion: II. Phase asymmetry. Journal of Neural Engineering, 8(6), 065004. doi:10.1088/1741-2560/8/6/065004

Stein, R. B., Misiaszek, J. E., & Pearson, K. G. (2000). Functional Role of Muscle Reflexes for Force Generation in the Decerebrate Walking Cat. The Journal of Physiology, 525(3), 781–791. doi:10.1111/j.1469-7793.2000.00781.x

Keywords: Aplysia, CpG, heteroclinic, homoclinic, saddle point

Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.

Presentation Type: Poster (but consider for student poster award)

Topic: Motor Systems

Citation: Shaw KM, Cullins MJ, Lu H, McManus JM, Thomas PJ and Chiel HJ (2012). Investigating localized sensitivity in the feeding patterns of Aplysia californica. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00323

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Received: 30 Apr 2012; Published Online: 07 Jul 2012.

* Correspondence: Mr. Kendrick M Shaw, Case Western Reserve University, Biology, Cleveland, OH, 44106, United States, kmshaw@mgh.harvard.edu