Computational Capabilities of Single Neurons: Relationship to Simple Forms of Associative and Nonassociative Learning in Aplysia

doi:10.1016/S0079-7421(08)60108-5

Psychology of Learning and Motivation

Volume 23, 1989, Pages 31-63

https://doi.org/10.1016/S0079-7421(08)60108-5 Get rights and content

Publisher Summary

This chapter describes some of the consequences of incorporating single-cell models into a network consisting of multiple plastic cells. Synaptic transmission is by no means a simple process, and changes in the efficacy of synaptic transmission can be because of a number of factors acting either independently or in concert. Transmitter release can be considered the product of two variables. One is the number of vesicles of transmitter available for release (N) and the second is the probability of release (P). Factors affecting the number of vesicles include the synthesis of transmitter, the reuptake of released transmitter, and the mobilization of vesicles from storage or reserve pools to release sites in the presynaptic terminal. Changes in synaptic transmission need not be limited to strictly a pre- or a post-synaptic locus; they could occur at both loci.

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According to the reward-prediction error hypothesis (RPEH) of dopamine, the phasic activity of dopaminergic neurons in the midbrain signals a discrepancy between the predicted and currently experienced reward of a particular event. It can be claimed that this hypothesis is deep, elegant and beautiful, representing one of the largest successes of computational neuroscience. This paper examines this claim, making two contributions to existing literature. First, it draws a comprehensive historical account of the main steps that led to the formulation and subsequent success of the RPEH. Second, in light of this historical account, it explains in which sense the RPEH is explanatory and under which conditions it can be justifiably deemed deeper than the incentive salience hypothesis of dopamine, which is arguably the most prominent contemporary alternative to the RPEH.
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This chapter introduces a computational approach to evolutionary interpretations of animal-learning phenomena, with an emphasis upon Pavlovian conditioning. The approach combines a neurocomputational algorithm (NCA) and a genetic algorithm (GA). The NCA determined the functioning of neural processing elements constituting artificial neural networks (ANNs). The GA consisted of a neurodevelopmentally informed genotype-to-phenotype transformation, and a scheme for simulating selection and reproduction. The interstimulus interval (ISI) function and the variation of optimal ISIs across preparations were chosen as motivating phenomena. On this basis, generations of ANNs were each trained in Pavlovian forward-delay procedures with different ISIs (either 2, 4, 8, or 16 time steps) and conditional stimuli (either CS1 or CS2). Individual fitness of a network architecture was identified with performance under these procedures. A major finding was that mean population fitness increased as a negatively accelerated function of generations. Although ANNs in different populations had comparable fitnesses at the end of evolution, larger ANNs emerged with selection for longer ISIs. Also, the magnitude of the Baldwin Effect (high innate responding to CS-alone preexposure trials) decreased as the selected ISI increased. Finally, when ANNs were trained under ISIs different from the ancestral ones, performances simulated ISI functions whose optimal values corresponded to the selected ISIs. These results are consistent with a synthesis of general-process and biological-constraint approaches to learning.
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Previously, we developed a single-cell mathematical model of the sensory neurons in Aplysia (Gingrich & Byrne, 1985, 1987). This single-cell model accurately simulated many aspects of empirically observed neuronal plasticity that contribute to simple forms of nonassociative and associative learning. In the present study, we incorporated this empirically derived adaptive element into small networks and examined the ability of these networks to simulate second-order conditioning and blocking. When the single-cell model was incorporated into a three-cell network (Hawkins & Kandel, 1984), we found that constraints imposed by the empirical data limited the ability of the network to simulate both second-order conditioning and blocking. On the other hand, we found that the detailed descriptions of subcellular processes unmasked phenomena relevant to the simulation of blocking, that are not captured by less detailed models. We also incorporated the model of the sensory neuron into a lateral inhibition-type network consisting of five elements. This network successfully simulated both second-order conditioning and blocking more readily than the three-cell network.
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Computational Capabilities of Single Neurons: Relationship to Simple Forms of Associative and Nonassociative Learning in Aplysia

Publisher Summary

Trends in Neuroscience

Biophysical Journal

Trends in Neuroscience

Biophysical Journal

Brain Research Bulletin

Neurochemistry International

Biophysical Journal

Neuroscience Letters

Brain Research

Biophysical Journal

Brain Research

Comparative Biochemistry and Physiology

Possible roles of Ca++ and c AMP in activity-dependent facilitation, a mechanism for associative learning in Aplysia

Society for Neuroscience Abstracts

Aspects of the cellular mechanism of temporal specificity in conditioning in Aplysia: Preliminary evidence for Ca2+ influx as a signal of activity

Society for Neuroscience Abstracts

Activation of adenylate cyclase in Aplysia neural tissue by Ca2+/calmodulin, a candidate for an associative mechanism during conditioning

Society Neuroscience Abstracts

Learning and memory in Drosophila, studied with mutants

Cold Spring Harbor Symposia of Quantitative Biology

Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse

Journal of Physiology (London)

Calcium entry and transmitter release at voltage-clamped nerve terminals of squid

Journal of Physiology (London)

Morphological basis of short-term habituation in Aplysia

Journal of Neuroscience

Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia

Journal of Neurocytology

Modulation of membrane currents and excitability by serotonin and c AMP in pleural sensory neurons of Aplysia

Society for Neuroscience Abstracts

Random walks in biology

Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′ : 5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia

Journal of Neuroscience

Calcium-dependent regulation of brain adenylate cyclase

Advances in Cyclic Nucleotide Research

Synaptic facilitation and behavioral sensitization in Aplysia: Possible role of serotonin and cyclic AMP

Science

Calcium current activation kinetics in neurones of the snail Lymnea stagnalis

Journal of Physiology (London)

Calcium currents in internally perfused nerve cell bodies of Limnea stagnalis

Journal of Physiology (London)

Analysis of the synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica

Journal of Neurophysiology

Cellular analysis of associative learning

Physiological Review

Contribution of individual mechanoreceptor sensory neurons to defensive gill-withdrawal reflex in Aplysia

Journal of Neurophysiology

An analysis of dishabituation and sensitization of the gill-withdrawal reflex in Aplysia

International Journal of Neuroscience

Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica

Science

A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia

Proceedings of the National Academy of Sciences U.S.A.

Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia

Science

Inhibitor of adenosine 3′ : 5′-monophosphate-dependent protein kinase blocks presynaptic facilitation in Aplysia

Journal of Neuroscience

Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia

Science

Kinetics of calcium-dependent inactivation of calcium current in voltage-clamped neurones of Aplysia californica

Journal of Physiology (London)

A cellular mechanism for the temporal specificity of classical conditioning of the siphon-withdrawal response in Aplysia

Society for Neuroscience Abstracts

Associative learning of the gill and siphon withdrawal reflex in Aplysia: Interneurons mediating the unconditioned response

Society Neuroscience Abstracts

The mathematics of diffusion

Calcium tail currents in voltage-clamped intact nerve cell bodies of Aplysia californica

Journal of Physiology (London)

Simulation of nonassociative and associative neuronal modifications in Aplysia

Society for Neuroscience Abstracts

Simulation of synaptic depression, posttetanic potentiation and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia

Journal of Neurophysiology

Single-cell neuronal model for associative learning

Journal of Neurophysiology

Possible roles of Ca⁺⁺ and c AMP in activity-dependent facilitation, a mechanism for associative learning in Aplysia

Aspects of the cellular mechanism of temporal specificity in conditioning in Aplysia: Preliminary evidence for Ca²⁺ influx as a signal of activity

Activation of adenylate cyclase in Aplysia neural tissue by Ca²⁺/calmodulin, a candidate for an associative mechanism during conditioning