 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, July 14, 2004, 24(28):6315-6325; doi:10.1523/JNEUROSCI.0965-04.2004
Previous Article | Next Article
Behavioral/Systems/Cognitive
The Construction of Movement with Behavior-Specific and Behavior-Independent Modules
Jian Jing, Elizabeth C. Cropper, Itay Hurwitz, andKlaudiusz R. Weiss Department of Physiology and Biophysics, Mount Sinai School of Medicine, New York, New York 10029-6574
Growing evidence suggests that different forms of complex motor acts are constructed through flexible combinations of a small number of modules in interneuronal networks. It remains to be established, however, whether a module simply controls groups of muscles and functions as a computational unit for use in multiple behaviors (behavior independent) or whether a module controls multiple salient features that define one behavior and is used primarily for that behavior (behavior specific). We used the Aplysia feeding motor network to examine the two proposals by studying the functions of identifiable interneurons. We identified three types of motor programs that resemble three types of behaviors that Aplysia produce: biting, swallowing, and rejection. Two ingestive programs (biting, swallowing) are defined by two movement parameters of the feeding apparatus (the radula): one is the same in both programs (phasing of radula closure motoneurons relative to radula protraction-retraction), whereas the other parameter (protraction duration) is different in the two programs. In each program, these two parameters were specified together by an individual neuron, but the neurons in each were different (B40 for biting, B30 for swallowing). These findings support the existence of behavior-specific modules. Furthermore, neuron B51 was found to mediate a phase that can be flexibly added on to both ingestive and egestive-rejection programs, suggesting that B51 may be a behavior-independent module. The functional interpretation of the role played by these modules is supported by the patterns of synaptic connectivity that they make. Thus, both behavior-specific and behavior-independent modules are used to construct complex behaviors.
Key words: module; modular organization; Aplysia; feeding; spinal system; motor programs; movement parameter coding; interneuron; central pattern generator
Received Jan 29, 2004; revised June 1, 2004; accepted June 2, 2004.
This article has been cited by other articles:
K. Sasaki, V. Brezina, K. R. Weiss, and J. Jing
Distinct Inhibitory Neurons Exert Temporally Specific Control over Activity of a Motoneuron ReceivingConcurrent Excitation and Inhibition
J. Neurosci., September 23, 2009; 29(38): 11732 - 11744.
[Abstract] [Full Text] [PDF]
J. Jing, F. S. Vilim, E. C. Cropper, and K. R. Weiss
Neural Analog of Arousal: Persistent Conditional Activation of a Feeding Modulator by Serotonergic Initiators of Locomotion
J. Neurosci., November 19, 2008; 28(47): 12349 - 12361.
[Abstract] [Full Text] [PDF]
T. Crow and L.-M. Tian
Sensory Regulation of Network Components Underlying Ciliary Locomotion in Hermissenda
J Neurophysiol, November 1, 2008; 100(5): 2496 - 2506.
[Abstract] [Full Text] [PDF]
A. Berkowitz
Physiology and Morphology of Shared and Specialized Spinal Interneurons for Locomotion and Scratching
J Neurophysiol, June 1, 2008; 99(6): 2887 - 2901.
[Abstract] [Full Text] [PDF]
K. Sasaki, J. Jing, M. R. Due, and K. R. Weiss
An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network
J. Neurosci., February 20, 2008; 28(8): 1916 - 1928.
[Abstract] [Full Text] [PDF]
J. Robbins, S. G. Butler, S. K. Daniels, R. Diez Gross, S. Langmore, C. L. Lazarus, B. Martin-Harris, D. McCabe, N. Musson, and J. Rosenbek
Swallowing and Dysphagia Rehabilitation: Translating Principles of Neural Plasticity Into Clinically Oriented Evidence
J Speech Lang Hear Res, February 1, 2008; 51(1): S276 - S300.
[Abstract] [Full Text] [PDF]
K. Sasaki, M. R. Due, J. Jing, and K. R. Weiss
Feeding CPG in Aplysia Directly Controls Two Distinct Outputs of a Compartmentalized Interneuron That Functions as a CPG Element
J Neurophysiol, December 1, 2007; 98(6): 3796 - 3801.
[Abstract] [Full Text] [PDF]
J.-s. Wu, M. R. Due, K. Sasaki, A. Proekt, J. Jing, and K. R. Weiss
State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network
J. Neurosci., October 3, 2007; 27(40): 10818 - 10831.
[Abstract] [Full Text] [PDF]
R. Nargeot, C. Petrissans, and J. Simmers
Behavioral and In Vitro Correlates of Compulsive-Like Food Seeking Induced by Operant Conditioning in Aplysia
J. Neurosci., July 25, 2007; 27(30): 8059 - 8070.
[Abstract] [Full Text] [PDF]
G. E. Serrano, C. Martinez-Rubio, and M. W. Miller
Endogenous Motor Neuron Properties Contribute to a Program-Specific Phase of Activity in the Multifunctional Feeding Central Pattern Generator of Aplysia
J Neurophysiol, July 1, 2007; 98(1): 29 - 42.
[Abstract] [Full Text] [PDF]
A. Berkowitz
Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex
J. Neurosci., April 25, 2007; 27(17): 4634 - 4641.
[Abstract] [Full Text] [PDF]
J. Jing, F. S. Vilim, C. C. Horn, V. Alexeeva, N. G. Hatcher, K. Sasaki, I. Yashina, Y. Zhurov, I. Kupfermann, J. V. Sweedler, et al.
From Hunger to Satiety: Reconfiguration of a Feeding Network by Aplysia Neuropeptide Y
J. Neurosci., March 28, 2007; 27(13): 3490 - 3502.
[Abstract] [Full Text] [PDF]
D. M. Neustadter, R. L. Herman, R. F. Drushel, D. W. Chestek, and H. J. Chiel
The kinematics of multifunctionality: comparisons of biting and swallowing in Aplysia californica
J. Exp. Biol., January 15, 2007; 210(2): 238 - 260.
[Abstract] [Full Text] [PDF]
D. A. Baxter and J. H. Byrne
Feeding behavior of Aplysia: A model system for comparing cellular mechanisms of classical and operant conditioning
Learn. Mem., November 1, 2006; 13(6): 669 - 680.
[Abstract] [Full Text] [PDF]
K. L. Briggman and W. B. Kristan Jr
Imaging dedicated and multifunctional neural circuits generating distinct behaviors.
J. Neurosci., October 18, 2006; 26(42): 10925 - 10933.
[Abstract] [Full Text] [PDF]
B. J. Norris, A. L. Weaver, L. G. Morris, A. Wenning, P. A. Garcia, and R. L. Calabrese
A Central Pattern Generator Producing Alternative Outputs: Temporal Pattern of Premotor Activity
J Neurophysiol, July 1, 2006; 96(1): 309 - 326.
[Abstract] [Full Text] [PDF]
Y. Zhurov and V. Brezina
Variability of motor neuron spike timing maintains and shapes contractions of the accessory radula closer muscle of Aplysia.
J. Neurosci., June 28, 2006; 26(26): 7056 - 7070.
[Abstract] [Full Text] [PDF]
H. Ye, D. W. Morton, and H. J. Chiel
Neuromechanics of Coordination during Swallowing in Aplysia californica
J. Neurosci., February 1, 2006; 26(5): 1470 - 1485.
[Abstract] [Full Text] [PDF]
C. S. Lum, Y. Zhurov, E. C. Cropper, K. R. Weiss, and V. Brezina
Variability of Swallowing Performance in Intact, Freely Feeding Aplysia
J Neurophysiol, October 1, 2005; 94(4): 2427 - 2446.
[Abstract] [Full Text] [PDF]
V. C. K. Cheung, A. d'Avella, M. C. Tresch, and E. Bizzi
Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors
J. Neurosci., July 6, 2005; 25(27): 6419 - 6434.
[Abstract] [Full Text] [PDF]
A. d'Avella and E. Bizzi
Shared and specific muscle synergies in natural motor behaviors
PNAS, February 22, 2005; 102(8): 3076 - 3081.
[Abstract] [Full Text] [PDF]
Y. Zhurov, A. Proekt, K. R. Weiss, and V. Brezina
Changes of Internal State Are Expressed in Coherent Shifts of Neuromuscular Activity in Aplysia Feeding Behavior
J. Neurosci., February 2, 2005; 25(5): 1268 - 1280.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|