Working memory and fear conditioning

Abstract

In trace conditioning, a short interval is interposed between the termination of the conditioned stimulus (CS) and the onset of the unconditioned stimulus (US). In delay conditioning, the CS and US overlap. We here investigate the extent to which human classical fear conditioning depends on working memory. Subjects had to carry out an n-back task, requiring tracking an item 1 or 2 back in a sequentially presented list of numbers, while simultaneously being tested for their ability to associate auditory cues with shocks under a variety of conditions (single-cue versus differential; delay versus trace; no task versus 0-, 1-, and 2-back). Differential delay conditioning proved to be more resilient than differential trace conditioning but does show a reduction due to task interference similar in slope to that found in trace conditioning. Explicit knowledge of the stimulus contingency facilitates but does not guarantee trace conditioning. Only the single-cue delay protocol shows conditioning during the more difficult working memory task. Our findings suggest that the larger the cognitive demands on the system, the less likely conditioning occurs. A postexperimental questionnaire showed a positive correlation between conditioning and awareness for differential trace conditioning extinction. P avlovian conditioning is widely used to study associative learning in species ranging from mollusks to flies, rodents, monkeys, and humans (1-10). This form of learning involves the association of an initially neutral stimulus, the conditioned stimulus (CS), with a correlated meaningful stimulus, the unconditioned stimulus (US). An unresolved question concerns the extent to which certain forms of classical conditioning depend on higher-level cognitive processes, including selective attention, working memory, and awareness (11-17). Eye-blink conditioning is an associative learning paradigm where the role of explicit knowledge͞awareness is being investigated. The paradigm involves the association of an eye blink (a somatic motor response) with a previously meaningless stimuli (CS).Recent data showed that, in humans, associative trace conditioning of eye-blink responses requires awareness of the contingency between the CS (a tone) and the US (a puff of air to the eye), whereas this is not the case for delay conditioning (11,(18)(19)(20). In delay conditioning, the start of the US is temporally contiguous with the CS, whereas in trace conditioning, an interval is interposed between the end of the CS and the start of the US. Distracting subjects by having them perform a secondary task (for example, a verbal shadowing task) during a trace procedure prevents conditioning. Furthermore, subjects' ability to report the exact nature of the CS͞US relationship (e.g., ''I believe the tone came before the airpuff'') is greatly impaired with concurrent distraction during trace conditioning. Conversely, associative delay conditioning appears to be insensitive to distractors. Other experiments find that both trace and delay associative differentia...

The role of awareness in delay and trace fear conditioning in humans

“…Similar observations of learning without awareness have been found during Pavlovian fear conditioning (Bechara et al, 1995;Esteves, Parra, Dimberg, & Öhman, 1994;Knight et al, 2003). These studies suggest that contingency awareness does not influence differential CR expression during certain delay procedures , whereas awareness of stimulus relationships appears to facilitate trace fear conditioning and is correlated with CR expression during the extinction of trace conditioned fear (Carter, Hofstötter, Tsuchiya, & Koch, 2003).…”

“…SCRs were slightly larger on unperceived trace CS than on unperceived trace CS trials, and perhaps significant differences would have been observed had it not been for other factors that can influence conditioning. For example, trace procedures appear to be more difficult than delay conditioning, and increasing task difficulty often interferes with CR acquisition (Carter et al, 2003;Solomon & Groccia-Ellison, 1996;Thompson, Moyer, & Disterhoft, 1996). In addition, the duration of the trace CS was shortened to maintain the same interstimulus interval between CS onset and UCS presentation for the delay and trace procedures.…”

Genetic variability in nicotinic acetylcholine receptors and nicotine addiction: Converging evidence from human and animal research

“…In trace cued conditioning, an auditory CS is separated by an interval of time before mice receive a footshock US. Mice acquire a context-US and a CS-US association, but the insertion of a time interval between the CS and US requires working memory to be engaged [15]. Therefore, the hippocampus is required for both the context-US and CS-US associations [114,134].…”

Concomitant Deficits in Working Memory and Fear Extinction Are Functionally Dissociated from Reduced Anxiety in Metabotropic Glutamate Receptor 7-Deficient Mice

“…Instead, extinction treatment generates new (inhibitory) context-dependent learning (Bouton, 2002(Bouton, , 2004. In human subjects, concurrent working memory performance interferes with Pavlovian fear conditioning, indicating that fear response acquisition in humans is a learning phenomenon that may also depend on higher-level cognitive processes (Carter et al, 2003). Concurrence of deficits in working memory and conditioned fear extinction in mGluR7 Ϫ/Ϫ mice suggests that suppression of conditioned fear during extinction training may rely on working memory resources, similar to other forms of fear suppression in rats (Beckers et al, 2006).…”

“…Although the neurobehavioral basis of fear acquisition is well understood (Maren, 2001), less is known about mechanisms underlying extinction (Myers and Davis, 2002). Because extinction is now considered to be an active and context-dependent form of learning inhibiting the expression of conditioned fear responses (Bouton, 2002(Bouton, , 2004Rescorla, 2004), it may depend on higher-level cognitive processes similar to those involved in working memory (Carter et al, 2003).…”