Enhancement of type B and A photoreceptor inhibitory synaptic connections in conditioned Hermissenda

Intrinsic changes have been identified in isolated and intact type A and type B photoreceptors following classical conditioning of the nudibranch mollusk Hermissenda. Aspects of various intrinsic, nonsynaptic modifications are expressed by alterations in the excitability of identified photoreceptors in response to the conditioned stimulus. In addition to changes in cellular excitability, changes in synaptic strength between identified neurons have been proposed as a possible mechanism of associative learning in several invertebrate preparations. Here we report that classical conditioning produces differential effects upon the strength of inhibitory monosynaptic connections between identified pairs of type B and type A photoreceptors. The amplitude of IPSPs elicited by an action potential in the medial type B photoreceptor and recorded from medical type A photoreceptors was significantly enhanced in conditioned animals as compared to pseudorandom controls. In contrast, the amplitude of IPSPs elicited by an action potential in the lateral type B photoreceptor and recorded from lateral type A photoreceptors did not show significant synaptic enhancement following conditioning. These results provide additional evidence for differential effects of conditioning upon cellular modifications in identified type A and type B photoreceptors, and further indicate that multiple sites of cellular plasticity exist in the visual system of conditioned Hermissenda.

[1]  T. Crow,et al.  Down-regulation of protein kinase C and kinase inhibitors dissociate short- and long-term enhancement produced by one-trial conditioning of Hermissenda. , 1993, Journal of neurophysiology.

[2]  D. Alkon,et al.  Associative Behavioral Modification in Hermissenda: Cellular Correlates , 1980, Science.

[3]  D. Alkon,et al.  Regulation of short-term associative memory by calcium-dependent protein kinase , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Byrne,et al.  Examples of Mechanistic Analyses of Learning and Memory in Invertebrates , 1991 .

[5]  D L Alkon,et al.  Ultrastructure of photoreceptors in the eye ofHermissenda labelled with intracellular injections of horseradish peroxidase , 1979, Journal of neurocytology.

[6]  D. Alkon,et al.  Input and output changes of an identified neural pathway are correlated with associative learning in Hermissenda , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M. Waxham,et al.  Down-regulation of protein kinase C blocks 5-HT-induced enhancement in Hermissenda B photoreceptors , 1991, Neuroscience Letters.

[8]  T. Carew,et al.  Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. , 1991, Science.

[9]  T. Crow,et al.  Light paired with serotonin in vivo produces both short- and long-term enhancement of generator potentials of identified B-photoreceptors in Hermissenda , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[11]  T. Crow,et al.  Conditioned modification of phototactic behavior in Hermissenda. II. Differential adaptation of B-photoreceptors , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Crow,et al.  Inhibition of protein synthesis blocks long-term enhancement of generator potentials produced by one-trial in vivo conditioning in Hermissenda. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Daniel L. Alkon,et al.  Responses of Photoreceptors in Hermissenda , 1972, The Journal of general physiology.

[14]  D L Alkon,et al.  Memory storage and neural systems. , 1989, Scientific American.

[15]  T. Crow,et al.  Differential expression of correlates of classical conditioning in identified medial and lateral type A photoreceptors of Hermissenda , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  D. A. Baxter,et al.  Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation in sensorimotor connections of Aplysia. , 1992, Journal of neurophysiology.

[17]  E. Walters,et al.  Long-term expansion and sensitization of mechanosensory receptive fields in Aplysia support an activity-dependent model of whole-cell sensory plasticity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  E. Kandel,et al.  Facilitatory transmitters and cAMP can modulate accommodation as well as transmitter release in Aplysia sensory neurons: Evidence for parallel processing in a single cell. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. A. Baxter,et al.  Differential effects of cAMP and serotonin on membrane current, action-potential duration, and excitability in somata of pleural sensory neurons of Aplysia. , 1990, Journal of neurophysiology.

[20]  T. Crow,et al.  Retention of an associative behavioral change in Hermissenda. , 1978, Science.

[21]  J Farley,et al.  Associative learning changes intrinsic to Hermissenda type A photoreceptors. , 1990, Behavioral neuroscience.

[22]  T. Crow,et al.  Light paired with serotonin mimics the effect of conditioning on phototactic behavior of Hermissenda. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. Alkon,et al.  Primary changes of membrane currents during retention of associative learning. , 1982, Science.

[24]  T. Crow Cellular and molecular analysis of associative learning and memory in Hermissenda , 1988, Trends in Neurosciences.

[25]  Jacob Cohen,et al.  Applied multiple regression/correlation analysis for the behavioral sciences , 1979 .

[26]  D L Alkon,et al.  Associative neural and behavioral change in Hermissenda: consequences of nervous system orientation for light and pairing specificity. , 1982, Journal of neurophysiology.

[27]  E. Walters,et al.  Multiple sensory neuronal correlates of site-specific sensitization in Aplysia , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[29]  D L Alkon,et al.  Primary changes of voltage responses during retention of associative learning. , 1982, Journal of neurophysiology.

[30]  D L Alkon,et al.  Sensory, interneuronal, and motor interactions within Hermissenda visual pathway. , 1984, Journal of neurophysiology.