Neural Network Approaches to Eyeblink Classical Conditioning

We have described our efforts to further the understanding of the neural substrates of rabbit eyeblink conditioning (in particular the cerebellum and hippocampus) through the use of neural networks. Over the years, the initial theoretical assumptions of the computational models have been maintained while more anatomically and physiologically detailed instantiations of these models have been developed. These neural networks have increased our understanding of how classical conditioning occurs in the cerebellum and hippocampus while making novel predictions which are guiding ongoing and future empirical studies. Neural networks result in simulations of various lesion conditions which offer subtle distinctions which may not be evident in a purely qualitative theory.

[1]  M. Garwicz,et al.  Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat , 2004, Experimental Brain Research.

[2]  P. Solomon,et al.  Hippocampus, context, and conditioning. , 1991, Behavioral neuroscience.

[3]  R. Rescorla,et al.  A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement , 1972 .

[4]  J. Bachevalier,et al.  Structural correlates and cellular mechanisms in entorhinal—hippocampal dysfunction , 1993, Hippocampus.

[5]  L. Kamin Predictability, surprise, attention, and conditioning , 1967 .

[6]  R. F. Thompson,et al.  Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. , 1998, Science.

[7]  P. Werbos,et al.  Beyond Regression : "New Tools for Prediction and Analysis in the Behavioral Sciences , 1974 .

[8]  Rodney Cotterill,et al.  Models of brain function , 1989 .

[9]  S. D. Berry,et al.  Medial septal lesions retard classical conditioning of the nicitating membrane response in rabbits. , 1979, Science.

[10]  W. R. Salafia,et al.  Retardation of rabbit nictitating membrane conditioning by subseizure electrical stimulation of hippocampus , 1979, Physiology & Behavior.

[11]  P. Solomon,et al.  The septohippocampal cholinergic system and classical conditioning of the rabbit's nictitating membrane response. , 1981, Journal of comparative and physiological psychology.

[12]  P. Solomon,et al.  Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. , 1975, Journal of comparative and physiological psychology.

[13]  R. C. Honey,et al.  Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. , 1993, Behavioral neuroscience.

[14]  JOHN W. Moore,et al.  Conditioned inhibition of the rabbit's nictitating membrane response , 1972 .

[15]  Richard F. Thompson,et al.  Sensorimotor learning and the cerebellum , 1991 .

[16]  Bernard Widrow,et al.  Adaptive switching circuits , 1988 .

[17]  P. Solomon,et al.  Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. , 1983, Science.

[18]  C. Malsburg Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[19]  R. Sutherland,et al.  The hippocampal formation is necessary for rats to learn and remember configural discriminations , 1989, Behavioural Brain Research.

[20]  S. Grossberg,et al.  Adaptive pattern classification and universal recoding: I. Parallel development and coding of neural feature detectors , 1976, Biological Cybernetics.

[21]  M. Hasselmo,et al.  A Computational Model of Cholinergic Disruption of Septohippocampal Activity in Classical Eyeblink Conditioning , 1996, Neurobiology of Learning and Memory.

[22]  B. Kosko,et al.  Visual Structures and Integrated Functions , 1991, Research Notes in Neural Computing.

[23]  Catherine E. Myers,et al.  Further implications of a computational model of septohippocampal cholinergic modulation in eyeblink conditioning , 1998, Psychobiology.

[24]  J. Theios,et al.  Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). , 1972, Journal of comparative and physiological psychology.

[25]  N. Schmajuk,et al.  Occasion setting: Associative learning and cognition in animals. , 1998 .

[26]  C. Sotelo,et al.  Synaptology of the cerebello-olivary pathway. Double labelling with anterograde axonal tracing and GABA immunocytochemistry in the rat , 1989, Brain Research.

[27]  Mark A. Gluck,et al.  Adaptive Stimulus Representations: A Computational Theory of Hippocampal-Region Functions , 1992, NIPS.

[28]  J. Steinmetz,et al.  Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response , 1991, Brain Research.

[29]  W. R. Salafia,et al.  Disruption of rabbit (Oryctolagus cuniculus) nictitating membrane conditioning by posttrial electrical stimulation of hippocampus , 1977, Physiology & Behavior.

[30]  M. Bouton,et al.  Time and context effects on performance in a Pavlovian discrimination reversal , 1993 .

[31]  E. Kehoe A layered network model of associative learning: learning to learn and configuration. , 1988, Psychological review.

[32]  J E Steinmetz,et al.  Possible conditioned stimulus pathway for classical eyelid conditioning in rabbits. I. Anatomical evidence for direct projections from the pontine nuclei to the cerebellar interpositus nucleus. , 1992, Behavioral and neural biology.

[33]  Richard F. Thompson The neurobiology of learning and memory. , 1986, Science.

[34]  J. Houk,et al.  Somatotopic alignment between climbing fiber input and nuclear output of the cat intermediate cerebellum , 1987, The Journal of comparative neurology.

[35]  E. Kremer The Rescorla-Wagner model: losses in associative strength in compound conditioned stimuli. , 1978, Journal of experimental psychology. Animal behavior processes.

[36]  James Zackheim,et al.  A temporally sensitive recurrent network model of occasion setting. , 1998 .

[37]  J. W. Moore,et al.  Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response , 2004, Experimental Brain Research.

[38]  E. Kehoe,et al.  Summation and configuration in patterning schedules with the rat and rabbit , 1985 .

[39]  P. Solomon Role of the hippocampus in blocking and conditioned inhibition of the rabbit's nictitating membrane response. , 1977, Journal of comparative and physiological psychology.

[40]  S. Kaneko,et al.  Involvement of Postsynaptic G-proteins in Hippocampal Long-Term Potentiation , 1992, Brain research.

[41]  M. Hasselmo,et al.  Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[43]  I. Martin,et al.  Blocking Observed in Human Eyelid Conditioning , 1991, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[44]  B. Campbell,et al.  Punishment and aversive behavior , 1969 .

[45]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

[46]  M. Gluck,et al.  Dissociation of hippocampal and entorhinal function in associative learning: A computational approach , 1995, Psychobiology.

[47]  Geoffrey E. Hinton,et al.  Learning internal representations by error propagation , 1986 .

[48]  M. Gluck,et al.  Context, conditioning, and hippocampal rerepresentation in animal learning. , 1994, Behavioral neuroscience.

[49]  B J Anderson,et al.  Cerebellar and Brainstem Circuits Involved in Classical Eyeblink Conditioning , 1994, Reviews in the neurosciences.

[50]  J. Walkenbach,et al.  The Rescorla-Wagner Theory of Conditioning: A Review of the Literature , 1980 .

[51]  Teuvo Kohonen,et al.  Self-Organization and Associative Memory , 1988 .

[52]  M. Gluck,et al.  A computational perspective on dissociating hippocampal and entorhinal function , 1994, Behavioral and Brain Sciences.

[53]  Richard F. Thompson,et al.  Topics in learning and performance , 1972 .

[54]  M. Hasselmo Neuromodulation and cortical function: modeling the physiological basis of behavior , 1995, Behavioural Brain Research.

[55]  J Ambros-Ingerson,et al.  Simulation of paleocortex performs hierarchical clustering. , 1990, Science.

[56]  Catherine E. Myers,et al.  Cerebellar Substrates for Error Correction in Motor Conditioning , 2001, Neurobiology of Learning and Memory.

[57]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[58]  R. F. Thompson,et al.  Neuronal substrate of classical conditioning in the hippocampus , 1976, Science.

[59]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[60]  R. Rescorla,et al.  Associations in Pavlovian conditioned inhibition , 1977 .

[61]  T. S. Brown,et al.  Hippocampal lesions and shuttlebox avoidance behavior: a fear hypothesis. , 1972, Physiology & behavior.

[62]  J. Gray,et al.  Psychoarithmetic or pick your own? , 1994, Behavioral and Brain Sciences.

[63]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[64]  W. B. Orr,et al.  Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response , 1983, Behavioural Brain Research.

[65]  Richard F. Thompson,et al.  Integrating Behavioral and Biological Models of Classical Conditioning , 1989 .

[66]  R. C. Honey,et al.  Context-specific conditioning in the conditioned-emotional-response procedure. , 1990, Journal of experimental psychology. Animal behavior processes.

[67]  R. E. Lubow,et al.  The Context Effect: The Relationship Between Stimulus Preexposure and Environmental Preexposure Determines Subsequent Learning. , 1976 .

[68]  Masao Ito The Cerebellum And Neural Control , 1984 .

[69]  L. Jarrard On the use of ibotenic acid to lesion selectively different components of the hippocampal formation , 1989, Journal of Neuroscience Methods.

[70]  Richard E Thompson,et al.  Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning , 1997, Trends in Neurosciences.

[71]  R. C. Honey,et al.  Conditioning and contextual retrieval in hippocampal rats. , 1991, Behavioral neuroscience.

[72]  JOHN W. Moore,et al.  Conditioned inhibition of the rabbit nictitating membrane response as a function of CS-UCS interval , 1975 .

[73]  C. Harley,et al.  Ibotenate lesions of the hippocampus enhance latent inhibition in conditioned taste aversion and increase resistance to extinction in conditioned taste preference. , 1993, Behavioral neuroscience.

[74]  E. Kehoe,et al.  Compound conditioning of the rabbit’s nictitating membrane response: Test trial manipulations , 1986 .

[75]  M. M. Patterson,et al.  Fimbrial lesions and sensory preconditioning. , 1984, Behavioral neuroscience.

[76]  D. Lawrence,et al.  The transfer of a discrimination along a continuum. , 1952, Journal of comparative and physiological psychology.