Central localization of plasticity involved in appetitive conditioning in Lymnaea.

Learning to associate a conditioned (CS) and unconditioned stimulus (US) results in changes in the processing of CS information. Here, we address directly the question whether chemical appetitive conditioning of Lymnaea feeding behavior involves changes in the peripheral and/or central processing of the CS by using extracellular recording techniques to monitor neuronal activity at two stages of the sensory processing pathway. Our data show that appetitive conditioning does not affect significantly the overall CS response of afferent nerves connecting chemosensory structures in the lips and tentacles to the central nervous system (CNS). In contrast, neuronal output from the cerebral ganglia, which represent the first central processing stage for chemosensory information, is enhanced significantly in response to the CS after appetitive conditioning. This demonstrates that chemical appetitive conditioning in Lymnaea affects the central, but not the peripheral processing of chemosensory information. It also identifies the cerebral ganglia of Lymnaea as an important site for neuronal plasticity and forms the basis for detailed cellular studies of neuronal plasticity.

[1]  Claire Martin,et al.  Learning Modulation of Odor-Induced Oscillatory Responses in the Rat Olfactory Bulb: A Correlate of Odor Recognition? , 2004, The Journal of Neuroscience.

[2]  D. A. Baxter,et al.  In vitro analog of classical conditioning of feeding behavior in aplysia. , 2003, Learning & memory.

[3]  Richard F. Thompson,et al.  Neural substrates of eyeblink conditioning: acquisition and retention. , 2003, Learning & memory.

[4]  R. Menzel,et al.  Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honeybee antennal lobes , 2003, Neuroscience.

[5]  G. Gheusi,et al.  Olfactory processing in a changing brain. , 2003, Neuroreport.

[6]  Paul R. Benjamin,et al.  A Persistent Cellular Change in a Single Modulatory Neuron Contributes to Associative Long-Term Memory , 2003, Current Biology.

[7]  C. Harley,et al.  Early Odor Preference Learning in the Rat: Bidirectional Effects of cAMP Response Element-Binding Protein (CREB) and Mutant CREB Support a Causal Role for Phosphorylated CREB , 2003, The Journal of Neuroscience.

[8]  Kevin Staras,et al.  Endogenous and network properties of Lymnaea feeding central pattern generator interneurons. , 2002, Journal of neurophysiology.

[9]  R. Chase,et al.  Behavior and Its Neural Control in Gastropod Molluscs , 2002 .

[10]  Paul R. Benjamin,et al.  Critical Time-Window for NO–cGMP-Dependent Long-Term Memory Formation after One-Trial Appetitive Conditioning , 2002, The Journal of Neuroscience.

[11]  K. Daly,et al.  The generalization of an olfactory-based conditioned response reveals unique but overlapping odour representations in the moth Manduca sexta. , 2001, The Journal of experimental biology.

[12]  E R Kandel,et al.  The Contribution of Activity-Dependent Synaptic Plasticity to Classical Conditioning in Aplysia , 2001, The Journal of Neuroscience.

[13]  K. Staras,et al.  Multiple Types of Control by Identified Interneurons in a Sensory-Activated Rhythmic Motor Pattern , 2001, The Journal of Neuroscience.

[14]  B Ermentrout,et al.  Model for olfactory discrimination and learning in Limax procerebrum incorporating oscillatory dynamics and wave propagation. , 2001, Journal of neurophysiology.

[15]  R. Menzel Searching for the memory trace in a mini-brain, the honeybee. , 2001, Learning & memory.

[16]  K. Staras,et al.  A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. , 2000, Learning & memory.

[17]  Y. Fujito,et al.  Histological characterization of lip and tentacle nerves in Lymnaea stagnalis , 1999, Neuroscience Research.

[18]  K. Staras,et al.  Cellular Traces of Behavioral Classical Conditioning Can Be Recorded at Several Specific Sites in a Simple Nervous System , 1999, The Journal of Neuroscience.

[19]  K. Staras,et al.  In vitro appetitive classical conditioning of the feeding response in the pond snail Lymnaea stagnalis. , 1997, Journal of neurophysiology.

[20]  P. Benjamin,et al.  Modulatory role for the serotonergic cerebral giant cells in the feeding system of the snail, Lymnaea. I. Fine wire recording in the intact animal and pharmacology. , 1994, Journal of neurophysiology.

[21]  G. Kemenes,et al.  Modulatory role for the serotonergic cerebral giant cells in the feeding system of the snail, Lymnaea. II. Photoinactivation. , 1994, Journal of neurophysiology.

[22]  W. Moody,et al.  Evidence for a peripheral olfactory memory in imprinted salmon. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D L Alkon,et al.  Reduction of two voltage-dependent K+ currents mediates retention of a learned association. , 1985, Behavioral and neural biology.

[24]  C. Mccrohan Initiation of Feeding Motor Output by an Identified Interneurone in the Snail Lymnaea Stagnalis , 1984 .

[25]  O. Zaitseva,et al.  Sensory cells in the head skin of pond snails , 1981, Cell and Tissue Research.

[26]  E. Roubos,et al.  Sensory input to growth stimulating neuroendocrine cells of Lymnaea stagnalis , 2004, Cell and Tissue Research.

[27]  Y Kirino,et al.  Behavioral modulation induced by food odor aversive conditioning and its influence on the olfactory responses of an oscillatory brain network in the slug Limax marginatus. , 1998, Learning & memory.

[28]  M R Rosenzweig,et al.  Aspects of the search for neural mechanisms of memory. , 1996, Annual review of psychology.

[29]  G. Audesirk,et al.  One-trial reward learning in the snail Lymnea stagnalis. , 1984, Journal of neurobiology.