Different Brain Areas Are Involved in Memory Expression at Different Times from Training

doi:10.1006/nlme.1996.0050

Neurobiology of Learning and Memory

Volume 66, Issue 2, September 1996, Pages 97-101

https://doi.org/10.1006/nlme.1996.0050 Get rights and content

Abstract

Rats were trained in a step-down inhibitory avoidance task and tested for retention 1, 31, or 60 days later. Three to 7 days prior to testing, they were bilaterally implanted with cannulae in the CA₁region of the dorsal hippocampus and in the amygdaloid nucleus (H + A), in the entorhinal cortex (EC), and in the posterior parietal cortex (PPC). Ten minutes prior to testing, the animals received, through the cannulae, 0.5-μl microinfusions of vehicle (20% dimethyl-sulfoxide in saline) or of 0.5 μg of CNQX dissolved in the vehicle. A second test session was carried out 90 min after the first. CNQX blocked retention test performance when given into H + A 1 day after training but not later; when given into EC 1 or 31 days after training, but not later; and when given into PPC 1, 31, or 60 days after training. In all cases performance returned to normal levels in the second test session. The data suggest that H and A are involved in memory expression for only a few days after acquisition; that EC is involved in memory expression for up to 31, but less than 60, days after acquisition; and that PPC is involved in memory expression for up to at least 2 months after acquisition.

References (0)

Cited by (41)

Unraveling Molecular and System Processes for Fear Memory
2022, Neuroscience
Citation Excerpt :
However, this cortical delay does not occur in the retrosplenial cortex (RSC) (Mello e Souza et al., 1999) or the frontal association cortex (FrA) (Mello e Souza et al., 2000b), as discussed later. The hippocampus is always essential for recalling recent declarative LTM, but not necessarily for remote LTM (Quillfeldt et al., 1994, 1996; Frankland and Bontempi, 2005; Quillfeldt, 2019). One possible interpretation is that memory is rapidly formed not only in the medial temporal lobe but also in other cortical regions.
For decades, Izquierdo and colleagues contributed to building the notion that declarative memory requires different processes at the molecular and systems levels. This review aims to discuss part of Izquierdo’s legacy, mainly but not exclusively that related to fear memory. First, some of the philosophical and evolutionary issues that arise from declarative memory definition are presented. Then, the underlying processes of declarative memory are depicted, discussing the formation, the nature and the progression of the memory trace in short-term and long-term memory, and describing the involvement of some molecular cascades in the hippocampal formation, mesocortex and frontal areas. Potential contributions to therapy or understanding cognitive processes are mentioned.
The blockade of the serotoninergic receptors 5-HT5A, 5-HT6 and 5-HT7 in the basolateral amygdala, but not in the hippocampus facilitate the extinction of fear memory
2019, Behavioural Brain Research
Citation Excerpt :
Modulation and storage are not necessarily mutually exclusive functions, and many studies believe that the BLA exerts both [25,35,36]. It operates to a certain extent in parallel with the CA1 region in memory processing [1,37], but there is evidence that BLA promotes learning, such as inhibitory avoidance, independently of hippocampus by increasing the emotional value of the training [38]. Animals treated with 5,7-dihydroxytryptamine (a serotonin-depleting agent) injected into the BLA showed increased duration of social interaction time, suggestive of reduced anxiety-like behavior, reduced acquisition of fear during conditioning and reduced fear retrieval [39].
Extinction is the learned inhibition of retrieval. It is the mainstay of exposure therapy, which is widely used to treat drug addiction, phobias and fear-related pathologies such as post-traumatic stress disorder. The serotonin (5-HT) system is positioned to modulate the extinction circuitry via ascending 5-HT projections that innervate certain brain structures including the hippocampus and the basolateral amygdala (BLA). The most recently described serotoninergic receptors 5-HT5A, 5-HT6, 5-HT7 affect different memory processes and so are putative therapeutic targets for disorders related to cognition; however, their role in the extinction of contextual fear conditioning (CFC) has not been studied yet. Here we investigate the role of these receptors in the CA1 region of the hippocampus and the BLA in the extinction of CFC. For this, male rats were implanted with cannulae in the CA1 or in the BLA region through which they received immediately or 3 h after extinction training of CFC infusions of SB699551 (10 μg/side), 5-HT5A antagonist; WAY-208466 (0.04 μg/side), 5-HT6 agonist; SB-271046A (10 μg/side), 5-HT6 antagonist; AS-19 (5 μg/side), 5-HT7 agonist; SB-269970 (5 μg/side), 5-HT7 antagonist. After 24 h, animals were submitted to a 3 min extinction test. Results show that the infusion immediately after extinction training of 5-HT5A, 5-HT6 and 5-HT7 antagonists, and 3 h after extinction training of 5-HT5A and 5-HT7 antagonists in the BLA region, but not in CA1, facilitates the extinction of CFC memory.
ACC Theta Improves Hippocampal Contextual Processing during Remote Recall
2019, Cell Reports
Citation Excerpt :
Thus, it is reasonable to conclude that the present results should extend to all tasks regardless of motivational valence, but certainly, this needs further experimentation to determine. Although studies in animal models suggest that different memory networks are engaged in encoding and remote recall (Quillfeldt et al., 1996; Takehara et al., 2003), this idea is based on changes in memory recall dependence from the HC for recent memories (Squire and Alvarez, 1995; Bayley et al., 2003; Frankland et al., 2006; Ding et al., 2008) to the medial frontal cortex for remote (Maviel et al., 2004; Blum et al., 2006). However, imaging and recording studies in humans report similar networks of structures are activated during both memory encoding or recent recall and retrieval (Piolino et al., 2004; Viard et al., 2007, 2010; Rugg and Vilberg, 2013; Conejo et al., 2013; Kragel et al., 2017).
Consolidation studies show that, over time, memory recall becomes independent of the medial temporal lobes. Multiple lines of research show that the medial frontal cortex, including the anterior cingulate cortex (ACC), is involved with contextual information processing and remote recall. We hypothesize that interactions between the ACC and hippocampal area CA1 will change as memories became more remote. Animals are re-exposed to multiple environments at different retention intervals. During remote recall, ACC-CA1 theta coherence increases, with the ACC leading area CA1. ACC theta regulates unit spike timing, gamma oscillations, and ensemble and single-neuron information coding in CA1. Over the course of consolidation, the strength and prevalence of ACC theta modulation grow, leading to richer environmental context representations in CA1. These data are consistent with the transference of contextual memory dependence to the ACC and indicate that remote memories are retrieved via ACC-driven oscillatory coupling with CA1.
Memory Modulation
2017, Learning and Memory: A Comprehensive Reference
This chapter reviews extensive evidence from both animal and human research indicating that stress hormones activated by emotional arousal modulate the consolidation of memory of recent experiences. The hormones interact with other neuromodulatory systems in influencing noradrenergic activation of the basolateral amygdala. The amygdala regulates the consolidation of different kinds of memory via its projections to other brain regions. This coordinated modulatory system serves to regulate the strength of memories in relation to their emotional significance. Stress hormones also influence memory retrieval and working memory. And, as with memory consolidation, their effects involve noradrenergic activation of the basolateral amygdala and its interactions with other brain regions.
Functional interactions between dentate gyrus, striatum and anterior thalamic nuclei on spatial memory retrieval
2015, Brain Research
Citation Excerpt :
In other words, the neural networks involved in recent memory storage are supposed to differ from those underlying remote memory. This fact is supported by lesion studies suggesting that inactivation of specific cortical regions would alter remote memory without disrupting a recent one (Quillfeldt et al., 1996; Takehara et al., 2003; Frankland et al., 2004). Moreover, the prefrontal cortex has been largely known for playing an important role in navigational tasks.
The standard model of memory system consolidation supports the temporal reorganization of brain circuits underlying long-term memory storage, including interactions between the dorsal hippocampus and extra-hippocampal structures. In addition, several brain regions have been suggested to be involved in the retrieval of spatial memory. In particular, several authors reported a possible role of the ventral portion of the hippocampus together with the thalamus or the striatum in the persistence of this type of memory. Accordingly, the present study aimed to evaluate the contribution of different cortical and subcortical brain regions, and neural networks involved in spatial memory retrieval. For this purpose, we used cytochrome c oxidase quantitative histochemistry as a reliable method to measure brain oxidative metabolism. Animals were trained in a hidden platform task and tested for memory retention immediately after the last training session; one week after completing the task, they were also tested in a memory retrieval probe. Results showed that retrieval of the previously learned task was associated with increased levels of oxidative metabolism in the prefrontal cortex, the dorsal and ventral striatum, the anterodorsal thalamic nucleus and the dentate gyrus of the dorsal and ventral hippocampus. The analysis of functional interactions between brain regions suggest that the dorsal and ventral dentate gyrus could be involved in spatial memory retrieval. In addition, the results highlight the key role of the extended hippocampal system, thalamus and striatum in this process. Our study agrees with previous ones reporting interactions between the dorsal hippocampus and the prefrontal cortex during spatial memory retrieval. Furthermore, novel activation patterns of brain networks involving the aforementioned regions were found. These functional brain networks could underlie spatial memory retrieval evaluated in the Morris water maze task.
How the amygdala affects emotional memory by altering brain network properties
2014, Neurobiology of Learning and Memory
Citation Excerpt :
However, comparable effects of post-training amygdala treatments have been obtained with many different kinds of training, including both high-arousing and low-arousing tasks, such as contextual fear conditioning (Lalumiere et al., 2003; Sacchetti, Lorenzini, Baldi, Tassoni, & Bucherelli, 1999; Vazdarjanova & McGaugh, 1999), cued fear conditioning (Hui et al., 2004; Roozendaal et al., 2006; Sacchetti et al., 1999; Schafe & LeDoux, 2000), Y-maze discrimination training (McGaugh, Introini-Collison, & Nagahara, 1988), change in reward magnitude (Salinas, Introini-Collison, Dalmaz, & McGaugh, 1997), conditioned place preference (Hsu, Schroeder, & Packard, 2002; Schroeder & Packard, 2003, 2004), radial-arm maze appetitive training (Packard & Chen, 1999), water-maze spatial and cued training (Packard & Teather, 1998; Packard, Cahill, & McGaugh, 1994), conditioned taste aversion (Miranda, LaLumiere, Buen, Bermudez-Rattoni, & McGaugh, 2003; Miranda, Quirarte, Rodriguez-Garcia, McGaugh, & Roozendaal, 2008), olfactory training (Kilpatrick & Cahill, 2003a), object recognition (Roozendaal, Okuda et al., 2006), extinction of contextual fear conditioning (Berlau & McGaugh, 2006), and extinction of conditioned reward (Schroeder & Packard, 2003). As these different training experiences are known to engage different brain systems (Gold, 2004; Izquierdo & Medina, 1997; McGaugh, 2002; Packard & Cahill, 2001; Packard & Knowlton, 2002; Quillfeldt et al., 1996; Zanatta et al., 1996), the BLA-induced modulation no doubt involves influences on information processing occurring in these different brain regions. Packard and colleagues (Packard et al., 1994; Packard & Teather, 1998) were the first to show that the amygdala can modulate memory processes in both the striatum (caudate nucleus) and hippocampus.
The amygdala has long been known to play a key role in supporting memory for emotionally arousing experiences. For example, classical fear conditioning depends on neural plasticity within this anterior medial temporal lobe region. Beneficial effects of emotional arousal on memory, however, are not restricted to simple associative learning. Our recollection of emotional experiences often includes rich representations of, e.g., spatiotemporal context, visceral states, and stimulus–response associations. Critically, such memory features are known to bear heavily on regions elsewhere in the brain. These observations led to the modulation account of amygdala function, which postulates that amygdala activation enhances memory consolidation by facilitating neural plasticity and information storage processes in its target regions. Rodent work in past decades has identified the most important brain regions and neurochemical processes involved in these modulatory actions, and neuropsychological and neuroimaging work in humans has produced a large body of convergent data. Importantly, recent methodological developments make it increasingly realistic to monitor neural interactions underlying such modulatory effects as they unfold. For instance, functional connectivity network modeling in humans has demonstrated how information exchanges between the amygdala and specific target regions occur within the context of large-scale neural network interactions. Furthermore, electrophysiological and optogenetic techniques in rodents are beginning to make it possible to quantify and even manipulate such interactions with millisecond precision. In this paper we will discuss that these developments will likely lead to an updated view of the amygdala as a critical nexus within large-scale networks supporting different aspects of memory processing for emotionally arousing experiences.

View all citing articles on Scopus

¹: Jorge H. Medina is a visiting professor from the Laboratorio de Neurorreceptores, Instituto de Biologı́a Celular “Eduardo De Robertis,” Facultad de Medicina, Universidad de Buenos Aires, Argentina.

²: This work was supported by Fundação de Amparo a Pesquisa do Estado do Rio Grande do Sul (FAPERGS), Brazil. We thank M. Bianchin, R. Walz, and S. G. Petry for their help in some of the experiments. Address correspondence and reprint requests to: Dr. Ivan Izquierdo, Departamento de Bioquı́mica, Instituto de Biociencias, UFRGS (centro), 90046-900 Porto Alegre, RS, Brazil. Fax: +55 51 227 1343.

View full text

Rapid CommunicationDifferent Brain Areas Are Involved in Memory Expression at Different Times from Training

Abstract

Rapid Communication
Different Brain Areas Are Involved in Memory Expression at Different Times from Training