Trends in Cognitive Sciences
Volume 6, Issue 12, 1 December 2002, Pages 524-531
Journal home page for Trends in Cognitive Sciences

Review
Classical conditioning, awareness, and brain systems

https://doi.org/10.1016/S1364-6613(02)02041-7Get rights and content

Abstract

Memory is composed of several different abilities that are supported by different brain systems. The distinction between declarative (conscious) and nondeclarative (non-conscious) memory has proved useful in understanding the nature of eyeblink classical conditioning – the best understood example of classical conditioning in vertebrates. In delay conditioning, the standard procedure, conditioning depends on the cerebellum and brainstem and is intact in amnesia. Trace conditioning, a variant of the standard procedure, depends additionally on the hippocampus and neocortex and is impaired in amnesia. Recent studies have sharpened the contrast between delay and trace conditioning by exploring the importance of awareness. We discuss these new findings in relation to the brain systems supporting eyeblink conditioning and suggest why awareness is important for trace conditioning but not for delay conditioning.

Section snippets

Brain substrates for delay and trace eyeblink conditioning

Work with rabbits first demonstrated a clear distinction between delay and trace eyeblink conditioning. The acquisition and retention of delay eyeblink conditioning require the cerebellum and associated brainstem structures [12]; no forebrain structures (including the hippocampus) are required. Thus, decerebrate rabbits with no remaining forebrain tissue (i.e. after removal of cerebral cortex, basal ganglia, limbic system, thalamus, and hypothalamus) exhibited normal retention of delay eyeblink

Awareness and differential eyeblink conditioning

In delay and trace differential conditioning, the CS+ (e.g. a tone) is followed by the US whereas the CS (e.g. a static noise) is presented alone. Successful differential conditioning occurs when more CRs are elicited by the CS+ than by the CS. In differential conditioning, the participant can in principle learn several different facts about the stimulus contingencies (for example, the CS+ predicts the US, the CS does not predict the US, and the CS+ and CS are unrelated), and knowledge

Remaining issues concerning differential eyeblink conditioning

These studies suggest that awareness of the stimulus contingencies is important for successful differential trace conditioning but is unnecessary for differential delay conditioning. Nevertheless, it is possible to construct differential delay conditioning protocols where awareness is related to successful conditioning. Particularly interesting are two studies where tones (800 Hz and 2100 Hz), rather than a tone and static noise, served as the CS+ and CS. Individuals who were identified as

Awareness and single-cue eyeblink conditioning

In single-cue conditioning, only one CS is presented, and the level of conditioning is determined by the number of trials in which a CR occurs. The relationship of awareness to single-cue conditioning was not evaluated systematically in earlier studies of eyeblink conditioning because most participants (especially the young adults typically studied) became aware of the simple contingency (the CS predicts the US). Nevertheless, early investigators viewed single-cue delay conditioning as simple

Expectancy of the US and delay and trace conditioning

The findings reviewed here suggest that delay and trace eyeblink conditioning are fundamentally different kinds of learning. Successful trace conditioning is related to the development of awareness (declarative knowledge) about the stimulus contingencies. By contrast, successful delay conditioning is unrelated to the development of awareness, at least in standard delay (or differential) paradigms where the CS (or the CS+ and CS) can be processed easily. Individuals who develop awareness of the

Conclusion

The studies outlined above can be understood in terms of the declarative and nondeclarative memory systems that support eyeblink classical conditioning. In both delay and trace conditioning paradigms, individuals sometimes develop declarative (conscious) knowledge about the stimulus contingencies, and sometimes do not. For the most commonly studied forms of delay conditioning, declarative knowledge is superfluous to the acquisition of the CR and conditioned performance can be supported by

Acknowledgements

The authors’ work reviewed herein was supported by the Medical Research Service of the Department of Veterans Affairs, NIMH grant 24650, and the Metropolitan Life Foundation. Joseph Manns is now at the Dept of Psychology, Boston University, Boston, MA 02215, USA.

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