A computational model of hippocampal function in trace conditioning

We introduce a new reinforcement-learning model for the role of the hippocampus in classical conditioning, focusing on the differences between trace and delay conditioning. In the model, all stimuli are represented both as unindividuated wholes and as a series of temporal elements with varying delays. These two stimulus representations interact, producing different patterns of learning in trace and delay conditioning. The model proposes that hippocampal lesions eliminate long-latency temporal elements, but preserve short-latency temporal elements. For trace conditioning, with no contiguity between cue and reward, these long-latency temporal elements are necessary for learning adaptively timed responses. For delay conditioning, the continued presence of the cue supports conditioned responding, and the short-latency elements suppress responding early in the cue. In accord with the empirical data, simulated hippocampal damage impairs trace conditioning, but not delay conditioning, at medium-length intervals. With longer intervals, learning is impaired in both procedures, and, with shorter intervals, in neither. In addition, the model makes novel predictions about the response topography with extended cues or post-training lesions. These results demonstrate how temporal contiguity, as in delay conditioning, changes the timing problem faced by animals, rendering it both easier and less susceptible to disruption by hippocampal lesions.

[1]  D. Whitteridge Lectures on Conditioned Reflexes , 1942, Nature.

[2]  I. Gormezano,et al.  CONDITIONING OF THE NICTITATING MEMBRANE OF THE RABBIT AS A FUNCTION OF CS-US INTERVAL. , 1964, Journal of Comparative and Physiological Psychology.

[3]  R. F. Thompson,et al.  Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. , 1986, Behavioral neuroscience.

[4]  M. M. Patterson,et al.  Retention and acquisition of classical trace conditioned responses by rabbits with hippocampal lesions. , 1986, Behavioral neuroscience.

[5]  Stephen Grossberg,et al.  Neural dynamics of adaptive timing and temporal discrimination during associative learning , 1989, Neural Networks.

[6]  Richard S. Sutton,et al.  Time-Derivative Models of Pavlovian Reinforcement , 1990 .

[7]  M. Gabriel,et al.  Learning and Computational Neuroscience: Foundations of Adaptive Networks , 1990 .

[8]  J. Disterhoft,et al.  Hippocampectomy disrupts trace eye-blink conditioning in rabbits. , 1990, Behavioral neuroscience.

[9]  N. Schmajuk,et al.  Stimulus configuration, classical conditioning, and hippocampal function. , 1992, Psychological review.

[10]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[11]  A. Machado Learning the temporal dynamics of behavior. , 1997, Psychological review.

[12]  J. Disterhoft,et al.  Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. , 1997, Journal of neurophysiology.

[13]  J. Disterhoft,et al.  Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat , 1999, Hippocampus.

[14]  M. Hasselmo,et al.  The hippocampus as an associator of discontiguous events , 1998, Trends in Neurosciences.

[15]  Richard S. Sutton,et al.  Introduction to Reinforcement Learning , 1998 .

[16]  E. Gould,et al.  Learning enhances adult neurogenesis in the hippocampal formation , 1999, Nature Neuroscience.

[17]  W. Levy,et al.  A model of hippocampal activity in trace conditioning: where's the trace? , 2001, Behavioral neuroscience.

[18]  Louis D. Matzel,et al.  The Role of the Hippocampus in Trace Conditioning: Temporal Discontinuity or Task Difficulty? , 2001, Neurobiology of Learning and Memory.

[19]  J. Disterhoft,et al.  Trace eyeblink conditioning is hippocampally dependent in mice , 2004, Hippocampus.

[20]  Tadashi Yamazaki,et al.  A Neural Network Model for Trace Conditioning , 2005, ICONIP.

[21]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[22]  Richard S. Sutton,et al.  Learning to predict by the methods of temporal differences , 1988, Machine Learning.

[23]  K. Allen,et al.  Dorsal, ventral, and complete excitotoxic lesions of the hippocampus in rats failed to impair appetitive trace conditioning , 2007, Behavioural Brain Research.

[24]  Richard S. Sutton,et al.  Stimulus Representation and the Timing of Reward-Prediction Errors in Models of the Dopamine System , 2008, Neural Computation.

[25]  P. I. Pavlov Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex. , 1929, Annals of Neurosciences.