Event Abstract

Back to Event

Sequential recruitment of identified I1/I3 motor neurons enhances muscle contraction through modulatory interactions

Hui Lu1*, Jeffrey M. McManus1, Miranda J. Cullins1 and Hillel J. Chiel2
  • 1 Case Western Reserve University, Biology, United States
  • 2 Case Western Reserve University, Biology, Neurosciences, Biomedical Engineering, United States

Previous studies have shown that motor neurons for a single muscle are recruited in an orderly fashion based on a ‘size principle’ to produce movements with different force and speed (Henneman, 1957; 1965a; 1965b; Mendell, 2005). Although sequential recruitment of motor neurons has been extensively studied in vertebrates during the past 50 years (Zajac and Faden, 1985; Gabriel et al, 2011; Mantilla and Sieck, 2011), it is difficult to study in vivo at the individual neuron level. To explore the behavioral significance and force outputs of motor neuron recruitment sequences, we studied it in the marine mollusk Aplysia californica, in which individual motor neurons can be identified, monitored and controlled.

Aplysia use the same feeding apparatus, the buccal mass, to perform multiple feeding behaviors: biting, swallowing and rejection. All feeding behaviors have two phases, protraction and retraction of the food grasper (radula/odontophore). Previous magnetic resonance imaging evidence (Neustadter et al, 2007) and our current data both suggest that the retraction phase is a major difference between biting and swallowing, and is primarily mediated by the contraction of the I1/I3 muscle. We found that buccal nerve 2 (BN2), which contains the axons of multiple I1/I3 motor neurons (e.g., B3, B6, B9, B10, B38, B39 and B43), is activated more intensely during the retraction phase in swallowing than in biting in vivo. In addition, identified I1/I3 motor neurons B3, B6 and B9 are more active in swallowing than in biting. Thus, we hypothesize that the increased retraction force during swallowing is due to the sequential recruitment of the identified I1/I3 motor neurons B6 and B9, followed by B3.

We found that BN2 neural activity of the I1/I3 motor neurons during retraction in vivo and in vitro can be divided into four sub-phases (blocks) based on the BN2 unit sizes, relative timing, bursting features, and muscle innervation. The B3, B6 and B9 neurons are activated during the middle blocks of the retraction phase in all three feeding behaviors. More specifically, B6 and B9 fire in both the second and third blocks of retraction, whereas B3 only fires in the third block. The duration and force of retraction are both primarily determined by the second and third blocks containing B3, B6 and B9. In addition, we found that the frequency range (10-15 Hz) of B3 firing in vivo is not high enough to generate large forces. However, the activation of B6 and B9 prior to B3 can enhance the I1/I3 muscle contraction evoked by B3, consistent with the modulatory effects from B9 to B3 (Keating and Lloyd, 1999), which could be caused by the small cardioactive peptide (SCP) released by B6 and B9 (Church and Lloyd, 1991; Weiss et al, 1992). Moreover, we found that repetitive activation of a single motor neuron, B3, B6, or B9, can also increase its own forces. Therefore, the sequential recruitment of B6 and B9, prior to B3, enhances muscle contraction through modulatory interactions both within single responses and from response to response.

Acknowledgements

This research was funded by NIH Grant NS047073 and NSF Grant DMS1010434.

References

1. Henneman E. Relation between size of neurons and their susceptibility to discharge. Science 126: 1345–1347, 1957.
2. Henneman E, Somjen G, and Carpenter DO. Excitability and inhibitability of motoneurons of different sizes. J Neurophysiol 28: 599–620, 1965a.
3. Henneman E, Somjen G, and Carpenter DO. Functional significance of cell size in spinal motoneurons. J Neurophysiol 28: 560–580, 1965b.
4. Mendell, L.M. The size principle: a rule describing the recruitment of motoneurons. J. Neurophysiol. 93: 3024–3026, 2005.
5. Zajac FE and Faden JS. Relationship among recruitment order, axonal conduction velocity, and muscle-unit properties of type-identified motor units in cat plantaris muscle. J Neurophysiol 53: 1303–1322, 1985.
6. Gabriel JP, Ausborn J, Ampatzis K, Mahmood R, Eklöf-Ljunggren E, and EI Manira A. Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci. 14 : 93-9, 2011.
7. Mantilla CB and Sieck GC. Phrenic motor unit recruitment during ventilatory and non-ventilatory behaviors. Respir Physiol Neurobiol. 179 : 57-63, 2011
8. Neustadter DM, Herman RL, Drushel RF, Chestek DW, and Chiel HJ. The kinematics of multifunctionality: comparisons of biting and swallowing in Aplysia californica. J Exp Biol. 210 : 238-60, 2007.
9. Keating C and Lloyd PE. Differential modulation of motor neurons that innervate the same muscle but use different excitatory transmitters in aplysia. J Neurophysiol. 82 : 1759-67, 1999.
10. Church and Lloyd. Expression of diverse neuropeptide cotransmitters by identified motor neurons in Aplysia. J. Neurosci. 11 : 618-25, 1991.
11. Weiss KR, Brezina V, Cropper EC, Hooper SL, Miller MW, Probst WC, Vilim FS, and Kupfermann I. Peptidergic co-transmission in Aplysia: functional implications for rhythmic behaviors. Experientia. 48 : 456-63, 1992.

Keywords: Aplysia, feeding, motor neuron, sequential recruitment

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: Lu H, McManus JM, Cullins MJ and Chiel HJ (2012). Sequential recruitment of identified I1/I3 motor neurons enhances muscle contraction through modulatory interactions. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00287

Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters.

The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated.

Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed.

For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions.

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

* Correspondence: Ms. Hui Lu, Case Western Reserve University, Biology, Cleveland, OH, 44106, United States, hxl75@case.edu