Timing of Fear Expression in Trace and Delay Conditioning Measured by Fear-Potentiated Startle in Rats

Abstract

In two experiments, the time course of the expression of fear in trace (hippocampus-dependent) versus delay (hippocampus-independent) conditioning was characterized with a high degree of temporal specificity using fear-potentiated startle. In experiment 1, groups of rats were given delay fear conditioning or trace fear conditioning with a 3-or 12-sec trace interval between conditioned stimulus (CS) offset and unconditioned stimulus (US) onset. During test, the delay group showed fear-potentiated startle in the presence of the CS but not after its offset, whereas the trace groups showed fear-potentiated startle both during the CS and after its offset. Experiment 2 compared the time course of fear expression after trace conditioning with the time course in two delay conditioning groups: one matched to the trace conditioning group with respect to CS duration, and the other with respect to ISI. In all groups, fear was expressed until the scheduled occurrence of the US and returned to baseline rapidly thereafter. Thus, in both trace and delay fear conditioning, ISI is a critical determinant of the time course of fear expression. These results are informative as to the possible role of neural structures, such as the hippocampus, in memory processes related to temporal information.Although in Pavlovian delay conditioning presentations of the conditioned stimulus (CS) and the unconditioned stimulus (US) overlap, in trace conditioning a temporal gap or "trace" interval is interposed between the CS and the US. Even though eyeblink (i.e., skeletal) and fear (i.e., emotional) conditioning rely upon different neural substrates, the hippocampus has been shown to be critically involved in trace conditioning in both preparations (Moyer Jr. et al. 1990;McEchron et al. 1998;Quinn et al. 2002). Thus, the hippocampus is unlikely to be involved simply in the expression of the motoric or emotional responses associated with trace conditioning. Rather, given that trace (hippocampally dependent) and delay (hippocampally independent) conditioning differ solely with respect to the relative timing of CS and US presentation, the hippocampus would appear to be critically involved in mnemonic processes related to encoding the temporal relationship between the CS and the US. To understand hippocampal function, it is important, therefore, to characterize how the timing of conditioned responses in delay and trace conditioning relates to the timing of occurrences of the CS and US in training (see Quinn et al. 2002). In the current studies, this issue was addressed by using the acoustic startle reflex to assess the time course of the expression of conditioned fear after trace and delay conditioning.Some evidence supporting the contention that the hippocampus is involved in the temporal aspects of memory for trace conditioning is derived from the finding that hippocampal lesions sometimes simply cause a diminution in the latency and amplitude of conditioned eyeblink responses, rather than an outright block of trace eyeblink conditioning (Port et al...

Hippocampal and cerebellar single-unit activity during delay and trace eyeblink conditioning in the rat

“…It should be noted that equivalent rates of delay and trace conditioning and equivalent asymptotes, when the trace interval is short, have been reported by others. For example, Kehoe and Napier (1991), using rabbits, found similar rates of 400-ms delay and 400-ms trace eyeblink conditioning with a 300-ms trace interval and Burman and Gewirtz (2004) reported equivalent fear after 7-sec delay and 7-sec trace fear conditioning with a 3-sec trace interval when fear was assessed using fear-potentiated startle.…”

Avoidance of harm and anxiety: A role for the nucleus accumbens

“…However, it is possible that having a delay between the CS and the US may result in an increase in anticipatory anxiety, since there is a period of potential uncertainty regarding whether the participant will get punished or not. Indeed, it has been shown that the delay between the CS and the US is a critical determinant of the time course of fear expression, and that after learning fear continues to be expressed after the presentation of the CS until the scheduled occurrence of the US (Burman and Gewirtz, 2004). Therefore, future work needs to directly compare the effect of different delay intervals on avoidance behavior, and how that may be expressed at the neuronal level.…”

Trace and long-delay fear conditioning in the developing rat

“…Cole, Barnet, and Miller (1995) have argued that the typically observed behavioral inferiority of trace, relative to shortdelay, conditioning reflects the expression of different temporal information encoded in the associations between CSs and USs, rather than inferior learning per se after trace conditioning (see also Burman & Gewirtz, 2004;Kehoe & Weidemann, 1999). Specifically, Cole et al suggested that rats learn ISIs between CSs and USs and that the learning of a long ISI (as in trace conditioning) is expressed as a behavioral deficit, and they provided evidence of substantial learning following trace conditioning when measured indirectly with second-order and sensory preconditioning.…”