We have reviewed research on the effects of stress on LTP in the hippocampus, amygdala and prefrontal cortex (PFC) and present new findings which provide insight into how the attention and memory-related functions of these structures are influenced by strong emotionality. We have incorporated the stress-LTP findings into our “temporal dynamics” model, which provides a framework for understanding the neurobiological basis of flashbulb and traumatic memories, as well as stress-induced amnesia. An important feature of the model is the idea that endogenous mechanisms of plasticity in the hippocampus and amygdala are rapidly activated for a relatively short period of time by a strong emotional learning experience. Following this activational period, both structures undergo a state in which the induction of new plasticity is suppressed, which facilitates the memory consolidation process. We further propose that with the onset of strong emotionality, the hippocampus rapidly shifts from a “configural/cognitive map” mode to a “flashbulb memory” mode, which underlies the long-lasting, but fragmented, nature of traumatic memories. Finally, we have speculated on the significance of stress-LTP interactions in the context of the Yerkes-Dodson Law, a well-cited, but misunderstood, century-old principle which states that the relationship between arousal and behavioral performance can be linear or curvilinear, depending on the difficulty of the task.

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We have studied the influence of predator stress (30 min of cat exposure) on long-term (24 h) spatial memory and the density of spines in basilar dendrites of CA1 neurons. Predator stress occurred either immediately before water maze training (Stress Pre-Training) or before the 24 h memory test (Stress Pre-Retrieval). The Control (nonstress) group exhibited excellent long-term spatial memory and a robust increase in the density of stubby, but not mushroom, shaped spines. The Stress Pre-Training group had impaired long-term memory and did not exhibit any changes in spine density. The Stress Pre-Retrieval group was also impaired in long-term memory performance, but this group exhibited an increase in the density of stubby, but not mushroom, shaped spines, which was indistinguishable from the control group. These findings indicate that: (1) A single day of water maze training under control conditions produced intact long-term memory and an increase in the density of stubby spines in CA1; (2) Stress before training interfered with the consolidation of information into long-term memory and suppressed the training-induced increase in spine density; and (3) Stress immediately before the 24 h memory test trial impaired the retrieval of the stored memory, but did not reverse the training-induced increase in CA1 spine density. Overall, this work provides evidence of structural plasticity in dendrites of CA1 neurons which may be involved in the consolidation process, and how spinogenesis and memory are modulated by stress.

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We have studied the effects of an acute predator stress experience on spatial learning and memory in adult male and female Sprague-Dawley rats. All rats were trained to learn the location of a hidden escape platform in the radial-arm water maze (RAWM), a hippocampus-dependent spatial memory task. In the control (non-stress) condition, female rats were superior to the males in the accuracy and consistency of their spatial memory performance tested over multiple days of training. In the stress condition, rats were exposed to the cat for 30 min immediately before or after learning, or before the 24-h memory test. Predator stress dramatically increased corticosterone levels in males and females, with females exhibiting greater baseline and stress-evoked responses than males. Despite these sex differences in the overall magnitudes of corticosterone levels, there were significant sex-independent correlations involving basal and stress-evoked corticosterone levels, and memory performance. Most importantly, predator stress impaired short-term memory, as well as processes involved in memory consolidation and retrieval, in male and female rats. Overall, we have found that an intense, ethologically relevant stressor produced a largely equivalent impairment of memory in male and female rats, and sex-independent corticosterone-memory correlations. These findings may provide insight into commonalities in how traumatic stress affects the brain and memory in men and women.Over a century of behavioral research has revealed a powerful influence of stress on learning and memory (James, 1890;Yerkes and Dodson 1908;Hebb 1955;McGaugh 2000). The literature in this area lacks consistency, however, with studies reporting that stress can enhance, impair, or have no effect on learning and memory (for reviews, see Conrad 2005;Diamond 2005;Lupien et al. 2005;Diamond et al. 2007). An added level of complexity in the stress-memory literature involves the influence of gender on stress-memory interactions (Shors 1998;Wolf et al. 2001;Wolf 2003;Cahill et al. 2004;Cahill 2006). Some research has indicated that stress can impair memory in men but not women (Wolf et al. 2001), but other work has shown that stress can enhance memory in women (Andreano and Cahill 2006). Stress has also been shown to produce opposite effects on the development of conditioned responses in classical conditioning in men and women. However, in contrast to the studies mentioned above, Jackson et al. (2005) reported that stress produced an enhancement of fear conditioning in men and an impairment in women. Finally, other work has demonstrated that stress or cortisol administration can impair memory in both men and women (Kirschbaum et al. 1996;de Quervain et al. 2000;Wolf et al. 2004).Studies investigating sex differences in stress-memory interactions in rodents have also produced inconsistent findings. Acute stress has been shown to impair spatial memory in male rats (Diamond et al. 1996(Diamond et al. , 19992006;Conrad et al. 2004;Sandi et al. 2005) and to enhance spatial...

Models of the neurobiology of memory have been based on the idea that information is stored as distributed patterns of altered synaptic weights in neuronal networks. Accordingly, studies have shown that post-training treatments that alter synaptic weights, such as the induction of long-term potentiation (LTP), can interfere with retrieval. In these studies, LTP induction has been relegated to the status of a methodological procedure that serves the sole purpose of disturbing synaptic activity in order to impair memory. This perspective has been expressed, for example, by Martin and Morris (2002: Hippocampus 12:609-636), who noted that post-training LTP impairs memory by adding "behaviorally meaningless" noise to hippocampal neural networks. However, if LTP truly is a memory storage mechanism, its induction should represent more than just a means with which to disrupt memory. Since LTP induction produces retrograde amnesia, the formation of a new memory should also produce retrograde amnesia. In the present report, we suggest that one type of learning experience, the storage of fear-related (i.e., stressful) memories, is consistent with this prediction. Studies have shown that stress produces potent effects on hippocampal physiology, generates long-lasting memories, and induces retrograde amnesia, all through mechanisms in common with LTP. Based on these findings, we have developed the hypothesis that a stressful experience generates an endogenous form of hippocampal LTP that substitutes a new memory representation for preexisting representations. In summary, our hypothesis implicates the induction of endogenous synaptic plasticity by stress in the formation of emotional memories and in retrograde amnesia.

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ABSTRACT:This speculative review serves two purposes. First, it as an extension of the ideas we developed in a previous review (Diamond et al., Hippocampus, 2004;14:281-291), and second, it is a rebuttal to Abraham's (Hippocampus, 2004;14:675-676) critique of that review. We had speculated on the functional significance of the finding that post-training LTP induction produces retrograde amnesia. We noted the similarities between the findings that strong tetanizing stimulation can produce LTP and retrograde amnesia, and that a strong emotional experience can produce a long-lasting memory and retrograde amnesia, as well. The commonalities between LTP induction and emotional learning provided the basis of our hypothesis that an emotional experience generates endogenous LTD/depotentiation, which reverses synaptic plasticity formed during previous learning experiences, and endogenous LTP, which underlies the storage of new information. Abraham raised several concerns with our review, including the criticism that our speculation ''falters because there is no evidence that stress causes LTD or depotentiation,'' and that research on stress and hippocampus has ''failed to report any LTP-like changes.'' Abraham's points are well-taken because stress, in isolation, does not appear to generate long-lasting changes in baseline measures of hippocampal excitability. Here, within the context of a reply to Abraham's critique, we have provided a review of the literature on the influence of stress, novelty, fear conditioning, and the retrieval of emotional memories on cognitive and physiological measures of hippocampal functioning. An emphasis of this review is our hypothesis that endogenous forms of depotentiation, LTD and LTP are generated only when arousing experiences occur in conjunction with memory-related activation of the hippocampus and amygdala. We conclude with speculation that interactions among the different forms of endogenous plasticity underlie a form of competition by synapses and memories for access to retrieval resources. V V C 2005 Wiley-Liss, Inc.