Reinstatement of conditioned fear and the hippocampus: an attentional-associative model

Abstract

An existing attentional-associative model of classical conditioning [Schmajuk N, Lam Y, Gray JA. Latent inhibition: a neural network approach. J Exp Psychol: Anim Behav Process 1996;22:321-49] is applied to the description of reinstatement in animals and humans. According to the model, inhibitory associations between the context (CX) and unconditioned stimulus (US) are formed during extinction, which help preserve the association between the conditioned stimulus (CS) and the US. However, summation and retardation tests fail to reveal these associations because (a) the CX is not attended or (b) a CX-CS configural stimulus formed during extinction is both poorly attended and weakly active during testing. When US presentations and testing occur in the same context, reinstatement is the consequence of a decreased CX inhibition and the increased attention to the CS, which activates the remaining CS-US association. When US presentations occur in the context of extinction but the CS is tested in a different context, reinstatement results from an increased attention to the CS and the combination of CS-CX and CX-US excitatory associations. The assumption that associations between CSs are impaired following neurotoxic hippocampal lesions or in amnesia, is sufficient to describe absence of reinstatement in those cases. However, additional assumptions might be needed to describe the effect of hippocampal lesions on other postextinction manipulations.

Figure 1. Block diagram of the Schmajuk-Lam-Gray (SLG; 1996) network

CS = conditioned stimulus; US = unconditioned stimulus; τ_CS = short-term memory trace of the CS; B_CS = prediction of the CS; z_CS = attentional memory; X_CS = internal representation of the CS; V_CS1-CS1, V _CS1-CS2, …,V_CS1-US = associations CS1-CS1, CS1-CS2, …, CS1-US; CR = conditioned response.

Figure 2. Reinstatement of conditioned fear in rats

Data indicate suppression ratios in different conditions. BC = backward conditioning, TC = reinstatement, CC = control group, TC-Ext = reinstatement and extinction group. Top Panel: Data from Bolles and Bouton (1979a, Experiments 1 and 2). Bottom Panel: Computer simulations. Average Suppression Ratio over 10 test trials.

Figure 3. Reinstatement of conditioned fear in rats

Data indicate Percent Freezing in groups conditioned and extinguished in Context A, presented with the US and tested in Contexts A or B. Top Panel: Data from Westbrook et al. (2002, Experiment 2). Bottom Panel: Computer simulations. Amplitude of the conditioned response on the first test trial.

Figure 4. Effect of neurotoxic lesions on reinstatement in rats

Top Panel: Data from Frohardt et al. (2000, Experiment 1) indicate suppression ratios following US presentations in the Same (TC) or Different (CC) context in animals receiving Sham or Hippocampal lesions. Bottom Panel: Computer simulations. Average Suppression Ratio over 7 test trials.

Figure 5. Reinstatement of conditioned fear in normal human participants and amnesic patients

Top Panel: Normalized skin conductance conditioned responses by group and experimental phase. Data from LaBar and Phelps (2005, Experiment 3). Bottom Panel: Computer simulations. Average conditioned responses over 2 trials.