Peter C. Holland

Amygdala circuitry in attentional and representational processes

The amygdala has long been implicated in the display of emotional behavior and emotional information processing, especially in the context of aversive events. In this review, we discuss recent evidence that links the amygdala to several aspects of food-motivated associative learning, including functions often characterized as attention, reinforcement and representation. Each of these functions depends on the operation of separate amygdalar subsystems, through their connections with other brain systems. Notably, very different processing systems seem to be mediated by the central nucleus and basolateral amygdala, subregions of the amygdala that differ in their anatomy and in their connectivity. The basolateral amygdala is involved in the acquisition and representation of reinforcement value, apparently through its connections with ventral striatal dopamine systems and with the orbitofrontal cortex. The dentral nucleus, however, contributes heavily to attentional function in conditioning, by way of its influence on basal forebrain cholinergic systems and on the dorsolateral striatum.

Hippocampus and context in classical conditioning

Recent evidence suggests that contextual learning encompasses a variety of changes in learning and performance processes. Only some of these changes depend on the hippocampus. Specialized functions proposed for the hippocampus in contextual learning include the construction and consolidation of contextual memory representations, incidental contextual learning, and inhibitory contextual learning.

The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior

Rats with neurotoxic lesions of the amygdala central nucleus (CN) were trained using appetitive Pavlovian conditioning procedures. Conditioned responses (CRs) that are representative of 2 classes of behavior were monitored. One type of CR resembled the orienting responses that were elicited by the conditioned stimuli (CSs) prior to pairing with food reinforcement: the other type of CR resembled the behavior elicited by food reinforcement itself. Holland (1977, 1984) has referred to these as CS-generated and unconditioned stimulus (US)-generated CRs, respectively. During differential conditioning, some lesioned and unlesioned rats received reinforced presentations of a visual cue and nonreinforced presentations of an auditory cue, and the others in each lesion condition received reinforced auditory and nonreinforced visual cue presentations. Relative to the control group, the CN-lesioned rats were impaired in the acquisition of CS-generated CRs to both visual and auditory CSs. Orienting responses and habituation to the CSs were, however, comparable for the lesion and control groups. Moreover, rats with CN lesions readily acquired the US-generated CRs. Thus, a specific class of conditioned behavior was impaired by CN damage. Many studies using aversive Pavlovian procedures have suggested that CN lesions impair fear conditioning. The present results suggest another role for CN in the conditioning of orienting/attentional responses.

Occasion setting : associative learning and cognition in animals

Analogies of Occasion Setting and Pavlovian Conditioning Conditional Learning - an Associative Analysis Mechanisms of Feature-Positive and Feature-Negative Discrimination Learning in an Appetitive Conditioning Paradigm What Can Nontraditional Features Tell Us About Conditioning and Occasion Setting? Pavlovian Feature-Ambiguous Discrimination Perspectives on Modulation - Modulator and Target Focused Views Contextual Control as Occasion Setting Hunger Cues as Modulatory Stimuli The Role of Attention in the Solution of Conditional Discrimination.

Event representation in Pavlovian conditioning: Image and action☆

In a typical Pavlovian conditioning experiment, a relatively insignificant event, the conditioned stimulus (CS), is paired with a biologically more meaningful event, the unconditioned stimulus (US). As a consequence of those pairings, the CS is thought to acquire response characteristics of the US. In this article I describe experiments with rats that suggest that under some circumstances, the CS acquires control of perceptual processing of the US, in the absence of that US itself. I present three kinds of evidence for this surrogate processing, which I liken to imagery or hallucination: (1) CSs come to control specific, sensory-evaluative responses normally evoked only by the USs; (2) CSs can substitute for USs in the establishment of new learning about those USs themselves; (3) CSs can substitute for USs in the modulation of conditioning to other events, either overshadowing (interfering) or potentiating learning, in the same manner as the USs themselves. Finally, I compare these data with evidence for conditioned sensation and imagery in humans, and suggest that imagery may be a very basic process, evolutionarily derived from perceptual and conditioning processes adapted to deal with remote or absent objects.

Amygdala Central Nucleus Lesions Disrupt Increments, But Not Decrements, in Conditioned Stimulus Processing

The effects of neurotoxic lesions of the amygdala central nucleus (CN) on changes in the associability of a conditioned stimulus (CS) in appetitive Pavlovian conditioning were examined in 2 experiments with rats. In Experiment 1, CN lesions had no effect on the reduction in the associability of a CS produced by preexposure to that cue (latent inhibition). In Experiment 2, CN lesions prevented the enhancement of the associability of a CS that is normally observed when an inconsistent predictive relation is arranged between that CS and another cue. The results support previous claims that the amygdala CN is involved in broad-based incremental, but not decremental, changes in the processing of CSs in Pavlovian conditioning.

Effects of amygdala central nucleus lesions on blocking and unblocking.

The effects of lesions of the amygdala central nucleus (CN) on blocking and unblocking of appetitive Pavlovian conditioning were examined in 2 experiments with rats. In both lesioned and unlesioned rats, prior pairing of one conditioned stimulus (CS) with a food unconditioned stimulus (US) blocked the acquisition of conditioning to a second CS when a compound of both stimuli was paired with that same US. If the value of the US was increased or decreased when the second CS was added, unlesioned rats acquired substantial conditioning to the second cue (unblocking). Unblocking occurred in lesioned rats only when the US value was increased. In both lesioned and unlesioned rats, unblocking was prevented if the compound cue was paired with the original US prior to the change in US value. These data suggest that the CN is involved in increasing attention to signals for significant events but not in tuning out redundant cues.

Transfer of negative occasion setting and conditioned inhibition across conditioned and unconditioned stimuli.

The transfer of negative occasion setting and conditioned inhibition across conditioned stimuli (CSs) and unconditioned stimuli (USs) was examined in four experiments that used Pavlovian appetitive feature negative discrimination training procedures with rats. After training with simultaneous compounds (A+, XA-), X inhibited conditioned responding (CRs) elicited by other CSs and CRs supported by other appetitive USs that had not been involved in discrimination training. After training with serial compounds (A+, X----A-), Xs power to set the occasion for nonresponding transferred across CSs and USs only if those events had also been involved in serial feature negative discrimination training. The results supported the suggestion that the acquisition of negative occasion setting involves the representation of individual events in a higher order memory system, separate from that involved in simple association, and that negative occasion setters act only on events that are represented in that system.

The effects of amygdala lesions on conditioned stimulus-potentiated eating in rats

Both control rats and rats with neurotoxic lesions of the amygdala central nucleus ate more food during presentations of a conditioned stimulus (CS) previously paired with food than during an unpaired CS. This potentiation occurred regardless of whether the food was presented in its usual place or in a different location. By contrast, rats with neurotoxic lesions of basolateral amygdala showed no evidence for conditioned potentiation of eating. These results are considered in the context of anatomical projections from these amygdalar areas to other brain regions involved in feeding, and the role of amygdala subregions in the acquisition of motivational value in conditioning.

Hippocampal lesions interfere with Pavlovian negative occasion setting

Rats were trained with either a serial feature positive (L→ T1+, T‐) or a serial feature negative (L→ T1‐, T1+) discrimination, intermixed with training on another, nonconditional discrimination (T2+, N‐), using a Pavlovian appetitive conditioning preparation with multiple response measures. Among rats trained with the serial feature positive discrimination, neurotoxic lesions of the hippocampus produced a transient impairment in the acquisition of that discrimination, but did not affect acquisition of the nonconditional discrimination. In contrast, among rats that received serial feature negative discrimination training, hippocampal lesions produced enduring deficits in the acquisition of both discriminations. The results of transfer tests indicated that both lesioned and control rats used a conditional learning strategy (occasion setting) to solve the feature positive and feature negative discriminations. Furthermore, lesioned rats, especially those that received training with the feature negative discrimination, displayed increasingly higher levels of general activity as training progressed. The results suggest that hippocampal lesions particularly interfere with inhibitory learning (negative occasion setting) about both explicit and contextual cues. Hippocampus 1999;9:143–157.