 |
Previous Article | Next Article 
Volume 17, Number 21,
Issue of November 1, 1997
pp. 8093-8105
Copyright ©1997 Society for Neuroscience
Contingent-Dependent Enhancement of Rhythmic Motor Patterns: An
In Vitro Analog of Operant Conditioning
Received June 30, 1997; accepted Aug. 11, 1997.
Romuald Nargeot,
Douglas A. Baxter, and
John H. Byrne
Department of Neurobiology and Anatomy, The University of Texas
Medical School at Houston, Houston, Texas 77030
Operant conditioning is characterized by the contingent
reinforcement of a designated behavior. Previously, feeding behavior in
Aplysia has been demonstrated to be modified by operant
conditioning, and a neural pathway (esophageal nerve; E n.) that
mediates some aspects of reinforcement has been identified. As a first
step toward a cellular analysis of operant conditioning, we developed an in vitro buccal ganglia preparation that expressed
the essential features of operant conditioning. Motor patterns that
represented at least two different aspects of fictive feeding (i.e.,
ingestion-like and rejection-like motor patterns) were elicited by
tonic stimulation of a peripheral buccal nerve (n.2,3). Three groups of
preparations were examined. In a contingent-reinforcement group,
stimulation of E n. was contingent on the expression of a specific type
of motor pattern (i.e., either ingestion-like or rejection-like). In a
yoke-control group, stimulation of E n. was not contingent on any
specific pattern. In a control group, E n. was not stimulated. The
frequency of the reinforced pattern increased significantly only in the
contingent-reinforcement group. No changes were observed in
nonreinforced patterns or in the motor patterns of the control and
yoke-control groups. Contingent reinforcement of the ingestion-like pattern was associated with an enhancement of activity in motor neuron
B8, and this enhancement was specific to the reinforced pattern. These
results suggest that the isolated buccal ganglia expressed an essential
feature of operant conditioning (i.e., contingent reinforcement
modified a designated operant) and that this analog of operant
conditioning is accessible to cellular analysis.
Key words:
buccal ganglia;
Aplysia californica;
central
pattern generator;
operant conditioning;
learning and memory;
contingent reinforcement
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]
|
 |
|

|
 |

|
 |
 
F. H. Sieling, C. C. Canavier, and A. A. Prinz
Predictions of Phase-Locking in Excitatory Hybrid Networks: Excitation Does Not Promote Phase-Locking in Pattern-Generating Networks as Reliably as Inhibition
J Neurophysiol,
July 1, 2009;
102(1):
69 - 84.
[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.-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]
|
 |
|

|
 |

|
 |
 
H.-Y. Koh and K. R. Weiss
Activity-Dependent Peptidergic Modulation of the Plateau-Generating Neuron B64 in the Feeding Network of Aplysia
J Neurophysiol,
February 1, 2007;
97(2):
1862 - 1867.
[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]
|
 |
|

|
 |

|
 |
 
T. Inoue, M. Murakami, S. Watanabe, Y. Inokuma, and Y. Kirino
In Vitro Odor-Aversion Conditioning in a Terrestrial Mollusk
J Neurophysiol,
June 1, 2006;
95(6):
3898 - 3903.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Diaz-Rios and M. W. Miller
Target-Specific Regulation of Synaptic Efficacy in the Feeding Central Pattern Generator of Aplysia: Potential Substrates for Behavioral Plasticity?
Biol. Bull.,
June 1, 2006;
210(3):
215 - 229.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. D. Hawkins, G. A. Clark, and E. R. Kandel
Operant Conditioning of Gill Withdrawal in Aplysia
J. Neurosci.,
March 1, 2006;
26(9):
2443 - 2448.
[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]
|
 |
|

|
 |

|
 |
 
Y. Zhurov, K. R. Weiss, and V. Brezina
Tight or Loose Coupling Between Components of the Feeding Neuromusculature of Aplysia?
J Neurophysiol,
July 1, 2005;
94(1):
531 - 549.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. D. Reyes, R. Mozzachiodi, D. A. Baxter, and J. H. Byrne
Reinforcement in an in vitro analog of appetitive classical conditioning of feeding behavior in Aplysia: Blockade by a dopamine antagonist
Learn. Mem.,
May 1, 2005;
12(3):
216 - 220.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Diaz-Rios and M. W. Miller
Rapid Dopaminergic Signaling by Interneurons That Contain Markers for Catecholamines and GABA in the Feeding Circuitry of Aplysia
J Neurophysiol,
April 1, 2005;
93(4):
2142 - 2156.
[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]
|
 |
|

|
 |

|
 |
 
C. C. Horn, Y. Zhurov, I. V. Orekhova, A. Proekt, I. Kupfermann, K. R. Weiss, and V. Brezina
Cycle-to-Cycle Variability of Neuromuscular Activity in Aplysia Feeding Behavior
J Neurophysiol,
July 1, 2004;
92(1):
157 - 180.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Brembs, D. A. Baxter, and J. H. Byrne
Extending In Vitro Conditioning in Aplysia to Analyze Operant and Classical Processes in the Same Preparation
Learn. Mem.,
July 1, 2004;
11(4):
412 - 420.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Kawai, T. Horikoshi, and M. Sakakibara
Involvement of the Ryanodine Receptor in Morphologic Modification of Hermissenda Type B Photoreceptors After In Vitro Conditioning
J Neurophysiol,
February 1, 2004;
91(2):
728 - 735.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Mozzachiodi, H. A. Lechner, D. A. Baxter, and J. H. Byrne
In Vitro Analog of Classical Conditioning of Feeding Behavior in Aplysia
Learn. Mem.,
November 1, 2003;
10(6):
478 - 494.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. C. Dembrow, J. Jing, A. Proekt, A. Romero, F. S. Vilim, E. C. Cropper, and K. R. Weiss
A Newly Identified Buccal Interneuron Initiates and Modulates Feeding Motor Programs in Aplysia
J Neurophysiol,
October 1, 2003;
90(4):
2190 - 2204.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Hurwitz, I. Kupfermann, and K. R. Weiss
Fast Synaptic Connections From CBIs to Pattern-Generating Neurons in Aplysia: Initiation and Modification of Motor Programs
J Neurophysiol,
April 1, 2003;
89(4):
2120 - 2136.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Katzoff, T. Ben-Gedalya, and A. J. Susswein
Nitric Oxide Is Necessary for Multiple Memory Processes after Learning That a Food Is Inedible in Aplysia
J. Neurosci.,
November 1, 2002;
22(21):
9581 - 9594.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Jing and K. R. Weiss
Interneuronal Basis of the Generation of Related but Distinct Motor Programs in Aplysia: Implications for Current Neuronal Models of Vertebrate Intralimb Coordination
J. Neurosci.,
July 15, 2002;
22(14):
6228 - 6238.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Brembs, F. D. Lorenzetti, F. D. Reyes, D. A. Baxter, and J. H. Byrne
Operant Reward Learning in Aplysia: Neuronal Correlates and Mechanisms
Science,
May 31, 2002;
296(5573):
1706 - 1709.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Sangha, C. McComb, A. Scheibenstock, C. Johannes, and K. Lukowiak
The effects of continuous versus partial reinforcement schedules on associative learning, memory and extinction in Lymnaea stagnalis
J. Exp. Biol.,
April 15, 2002;
205(8):
1171 - 1178.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. H. Elliott and A. J. Susswein
Comparative neuroethology of feeding control in molluscs
J. Exp. Biol.,
April 1, 2002;
205(7):
877 - 896.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Jing and K. R. Weiss
Neural Mechanisms of Motor Program Switching in Aplysia
J. Neurosci.,
September 15, 2001;
21(18):
7349 - 7362.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. V. Orekhova, J. Jing, V. Brezina, R. A. DiCaprio, K. R. Weiss, and E. C. Cropper
Sonometric Measurements of Motor-Neuron-Evoked Movements of an Internal Feeding Structure (the Radula) in Aplysia
J Neurophysiol,
August 1, 2001;
86(2):
1057 - 1061.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Xin, J. Koester, J. Jing, K. R. Weiss, and I. Kupfermann
Cerebral-Abdominal Interganglionic Coordinating Neurons in Aplysia
J Neurophysiol,
January 1, 2001;
85(1):
174 - 186.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Deodhar and I. Kupfermann
Studies of Neuromodulation of Oscillatory Systems in Aplysia, by Means of Genetic Algorithms
Adaptive Behavior,
June 1, 2000;
8(3-4):
267 - 296.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
H. A. Lechner, D. A. Baxter, and J. H. Byrne
Classical Conditioning of Feeding in Aplysia: I. Behavioral Analysis
J. Neurosci.,
May 1, 2000;
20(9):
3369 - 3376.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. A. Lechner, D. A. Baxter, and J. H. Byrne
Classical Conditioning of Feeding in Aplysia: II. Neurophysiological Correlates
J. Neurosci.,
May 1, 2000;
20(9):
3377 - 3386.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Brembs and M. Heisenberg
The Operant and the Classical in Conditioned Orientation of Drosophila melanogaster at the Flight Simulator
Learn. Mem.,
March 1, 2000;
7(2):
104 - 115.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
E. A. Kabotyanski, D. A. Baxter, S. J. Cushman, and J. H. Byrne
Modulation of Fictive Feeding by Dopamine and Serotonin in Aplysia
J Neurophysiol,
January 1, 2000;
83(1):
374 - 392.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Nargeot, D. A. Baxter, G. W. Patterson, and J. H. Byrne
Dopaminergic Synapses Mediate Neuronal Changes in an Analogue of Operant Conditioning
J Neurophysiol,
April 1, 1999;
81(4):
1983 - 1987.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Nargeot, D. A. Baxter, and J. H. Byrne
In Vitro Analog of Operant Conditioning in Aplysia. I. Contingent Reinforcement Modifies the Functional Dynamics of an Identified Neuron
J. Neurosci.,
March 15, 1999;
19(6):
2247 - 2260.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Nargeot, D. A. Baxter, and J. H. Byrne
In Vitro Analog of Operant Conditioning in Aplysia. II. Modifications of the Functional Dynamics of an Identified Neuron Contribute to Motor Pattern Selection
J. Neurosci.,
March 15, 1999;
19(6):
2261 - 2272.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. E. Spencer, N. I. Syed, and K. Lukowiak
Neural Changes after Operant Conditioning of the Aerial Respiratory Behavior in Lymnaea stagnalis
J. Neurosci.,
March 1, 1999;
19(5):
1836 - 1843.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Botzer, S. Markovich, and A. J. Susswein
Multiple Memory Processes Following Training That a Food Is Inedible in Aplysia
Learn. Mem.,
July 1, 1998;
5(3):
204 - 219.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
E. A. Kabotyanski, D. A. Baxter, and J. H. Byrne
Identification and Characterization of Catecholaminergic Neuron B65, Which Initiates and Modifies Patterned Activity in the Buccal Ganglia of Aplysia
J Neurophysiol,
February 1, 1998;
79(2):
605 - 621.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. D. Sanchez and M. D. Kirk
Short-Term Synaptic Enhancement Modulates Ingestion Motor Programs of Aplysia
J. Neurosci.,
July 15, 2000;
20(14):
RC85 - RC85.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|