reinforcement processing. Backward inhibitory learning in honeybees: a behavioral analysis of

Abstract One class of theoretical accounts of associative learning suggests that reinforcers are processed according to learning rules that minimize the predictive error between the expected strength of future reinforcement and its actual strength. The omission of reinforcement in a situation where it is expected leads to inhibitory learning of stimuli indicative for such a violation of the prediction. There are, however, results indicating that inhibitory learning can also be induced by other mechanisms. Here, we present data from olfactory reward conditioning in honeybees that show that (1) one- and multiple-trial backward conditioning results in conditioned inhibition (CI); (2) the inhibition is maximal for a 15-sec interval between US and CS; (3) there is a nonmonotonic dependency on the degree of CI from the US-CS interval during backward pairing; and (4) the prior association of context stimuli with reinforcement is not necessary for the development of CI. These results cannot be explained by models that only minimize a prediction error. Rather, they are consistent with models of associative learning that, in addition, assume that learning depends on the

[1]  James H. Marden,et al.  Floral choices by honeybees in relation to the relative distances to flowers , 1981 .

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

[3]  Joel L. Davis,et al.  A Model of How the Basal Ganglia Generate and Use Neural Signals That Predict Reinforcement , 1994 .

[4]  J. W. Moore,et al.  Conditioned response timing and integration in the cerebellum. , 1997, Learning & memory.

[5]  M. Spetch,et al.  Backward conditioning: a reevaluation of the empirical evidence. , 1981, Psychological bulletin.

[6]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  N. Donegan,et al.  Some Relationships Between a Computational Model (Sop) and a Neural Circuit for Pavlovian (Rabbit Eyeblink) Conditioning , 1989 .

[8]  B. H. Smith,et al.  An analysis of blocking in odorant mixtures: an increase but not a decrease in intensity of reinforcement produces unblocking. , 1997, Behavioral neuroscience.

[9]  M. Bitterman,et al.  Analysis of choice in honeybees , 1985 .

[10]  An analysis of variability in the feeding motor program of the honey bee; the role of learning in releasing a modal action pattern , 2010 .

[11]  B. H. Smith,et al.  The olfactory memory of the honeybee Apis mellifera. II. Blocking between odorants in binary mixtures. , 1994, The Journal of experimental biology.

[12]  M. Hammer,et al.  Learning and memory in the honeybee , 1995 .

[13]  A G Barto,et al.  Toward a modern theory of adaptive networks: expectation and prediction. , 1981, Psychological review.

[14]  J. Schull A Conditioned Opponent Theory of Pavlovian Conditioning and Habituation1 , 1979 .

[15]  M. Hammer An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees , 1993, Nature.

[16]  M. Hammer,et al.  Food-induced arousal and nonassociative learning in honeybees: dependence of sensitization on the application site and duration of food stimulation. , 1994, Behavioral and neural biology.

[17]  G. Bicker,et al.  Habituation of an appetitive reflex in the honeybee. , 1992, Journal of neurophysiology.

[18]  Karl J. Friston,et al.  Value-dependent selection in the brain: Simulation in a synthetic neural model , 1994, Neuroscience.

[19]  S. Maier,et al.  Conditioned inhibition and the UCS-CS interval , 1976, Animal learning & behavior.

[20]  H. Plotkin,et al.  Backward conditioning in the rabbit (Oryctolagus cuniculus). , 1975, Journal of comparative and physiological psychology.

[21]  N. Mackintosh A Theory of Attention: Variations in the Associability of Stimuli with Reinforcement , 1975 .

[22]  J. Overmier,et al.  Nonassociative habituation, US preexposure, and backward inhibitory conditioning with signaled and unsignaled USs , 1990 .

[23]  R. Solomon,et al.  An opponent-process theory of motivation. I. Temporal dynamics of affect. , 1974, Psychological review.

[24]  V. Lolordo,et al.  Role of safety in the Pavlovian backward fear conditioning procedure. , 1968, Journal of comparative and physiological psychology.

[25]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[26]  V. Rehder Quantification of the honeybee's proboscis reflex by electromyographic recordings , 1987 .

[27]  J. Konorski Conditioned reflexes and neuron organization. , 1948 .

[28]  R. Menzel,et al.  Memory dynamics and foraging strategies of honeybees , 2004, Behavioral Ecology and Sociobiology.

[29]  R. Malaka,et al.  Real-time models of classical conditioning , 1996, Proceedings of International Conference on Neural Networks (ICNN'96).

[30]  Peter Dayan,et al.  Bee foraging in uncertain environments using predictive hebbian learning , 1995, Nature.

[31]  L. R. Kipp The flight directionality of honeybees foraging on real and artificial inflorescences , 1987 .

[32]  P. Holland Event representation in Pavlovian conditioning: Image and action , 1990, Cognition.

[33]  M. Zimmerman Optimal foraging: Random movement by pollen collecting bumblebees , 1982, Oecologia.