Fear potentiated startle at short intervals following conditioned stimulus onset during delay but not trace conditioning OLE A ˚ SLI, SILJE KULVEDRØSTEN, LINE E. SOLBAKKEN, and MAGNE ARVE FLATEN Department of Psychology, University of Troms, Troms, Norway Abstract The latency of conditioned fear after delay and trace conditioning was investigated. Some argue that delay conditioning is not dependent on awareness. In contrast, trace conditioning, where there is a gap between the conditioned stimulus (CS) and the unconditioned stimulus (US), is assumed to be dependent on awareness. In the present study, a tone CS signaled a noise US presented 1000 ms after CS onset in the delay conditioning group. In the trace conditioning group, a 200-ms tone CS was followed by an 800-ms gap prior to US presentation. Fear-potentiated startle should be seen at shorter intervals after delay conditioning compared to trace conditioning. Analyses showed increased startle at 30, 50, 100, and 150 ms after CS onset following delay conditioning compared to trace conditioning. This implies that fear- relevant stimuli elicit physiological reactions before extended processing of the stimuli occur, following delay, but not trace conditioning. Descriptors: Emotion, Learning/memory, Unconscious processes, Normal volunteers, Startle blink Learning to predict danger from previous experience is necessary for an organism’s survival. Classical fear conditioning is one of the best understood experimental models for this form of learn- ing. In this model, a neutral conditioned stimulus (CS) is paired with an aversive unconditioned stimulus (US). After repeated pairings of the CS and US, the CS comes to elicit responses related to fear, for example, increased heart rate, skin conduc- tance responses, and potentiated startle. Augmented startle un- der fear is in many ways an ideal measure of experimental fear. It has a precise temporal resolution (Grillon & Baas, 2003) and seems to be less affected by fear irrelevant arousal (Hamm & Vaitl, 1996). The precise temporal resolution makes potentiated startle a well-suited alternative for measuring the latency of the conditioned fear response. The latency of conditioned fear may provide information on the degree of processing of the CS and the neural systems underlying conditioned fear. There is a debate about the role of awareness of the CS/US contingency in classical conditioning. Squire (2004; Manns, Clark, & Squire, 2001; Smith, Clark, Manns, & Squire, 2005) argued that single-cue delay eyeblink classical conditioning is independent of awareness of the CS/US contingency. It is argued that this form of conditioning is dependent on the cerebellum and, importantly, is independent of the hippocampus, as evi- denced by research showing that lesions to the anterior inter- positus nucleus impair learning (Clark, Zhang, & Lavond, 1992; Krupa, Thompson, & Thompson, 1993; Lavond, Kim, & Thompson, 1993), whereas hippocampal lesions do not impair learning (Berger & Orr, 1983; Schmaltz & Theios, 1972). Trace conditioning, on the other hand, where there is a temporal gap between the CS and the US (see Figure 1), is dependent on the hippocampus (Gabrieli et al., 1995; Solomon, Vander Schaaf, Thompson, & Weisz, 1986). Accordingly, whereas delay condi- tioning is cerebellum dependent, trace conditioning requires an intact hippocampus (Beylin et al., 2001). From another perspective, Lovibond and Shanks (2002b) argued that unconscious human conditioning had not been proven. Their main argument was that almost every study of the role of consciousness in classical conditioning used inadequate measures of awareness and that most measures tend to under- estimate awareness or that the experimental procedures used may lead to underestimated awareness (Lovibond & Shanks, 2002a, 2002b). A similar dissociation between conscious and unconscious processing is found in research on conditioned fear (Fanselow & Poulos, 2005). In delay fear conditioning to simple auditory CSs, an intact CS pathway from the medial geniculate nucleus of the thalamus to the dorsal portion of the lateral nucleus of the amygdala is sufficient for the expression of conditioned fear (LeDoux, Farb, & Romanski, 1991). The association between the CS and US seems to be formed in the amygdala without requiring involvement of cortical structures (Fanselow & Kim, 1994; Miserendino, Sananes, Melia, & Davis, 1990). Trace fear conditioning, on the other hand, requires hippocampal activity (McEchron, Bouwmeester, Tseng, Weiss, & Disterhoft, 1998; Address reprint requests to: Ole A ˚ sli, Department of Psychology, University of Troms, N-9037 Troms, Norway. E-mail: olea@psyk. uit.no Psychophysiology, 46 (2009), 880–888. Wiley Periodicals, Inc. Printed in the USA. Copyright r 2009 Society for Psychophysiological Research DOI: 10.1111/j.1469-8986.2009.00809.x 880