Time-limited role of the hippocampus in the memory for trace eyeblink conditioning in mice

Takehara, Kaori; Kawahara, Shigenori; Takatsuki, Kanako; Kirino, Yutaka

doi:10.1016/s0006-8993(02)03159-1

Cited by 90 publications

(86 citation statements)

References 40 publications

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“…These findings can be contrasted with the results that have typically been observed after hippocampal damage in tasks of nonspatial memory such as trace eyeblink conditioning (Kim et al, 1995;Takehara et al, 2002Takehara et al, , 2003, social transmission of food preference (Winocur, 1990;Winocur et al, 2001;Clark et al, 2002), and in tasks other than the water maze that appear to have a spatial component, such as contextual fear conditioning (Kim and Fanselow, 1992;Anagnostaras et al, 1999), but that do not require the animal to navigate to a specific point in space (for a discussion of this issue, see Clark et al, 2005). In all the studies just cited, as well as in others (for review, see Squire et al, 2004), hippocampal lesions made soon after training impaired performance, and lesions made at a later time had no effect.…”

Section: Discussionmentioning

confidence: 57%

Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life

2005

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Damage to the hippocampus typically produces temporally graded retrograde amnesia, whereby memories acquired recently are impaired more than memories acquired remotely. This phenomenon has been demonstrated repeatedly in a variety of species and tasks, and it has figured prominently in theoretical treatments of memory and hippocampal function. A striking exception to the finding of temporally graded retrograde amnesia comes from studies with rodents using spatial tasks like the water maze. In these studies, recent and remote memory were similarly impaired following hippocampal lesions. In contrast to work with rodents, studies of patients with medial temporal lobe lesions, including complete hippocampal lesions, indicate that remote spatial memory can be intact. One difference between studies in humans and studies in rodents is that spatial memory in animal studies is acquired during a limited period of time when the animals are adults. In contrast, the spatial memory studied in humans was acquired beginning at an early age and learning continued for a considerable period of time. We initiated training in a standard water maze immediately after rats had been weaned at 21 days of age and continued training until the rats were young adults (90 days old). Large hippocampal lesions were made 100 days after the completion of training. After recovery from surgery, control rats exhibited good retention on the first retention probe trial, but rats with hippocampal lesions performed at chance. Thus, even after extended training beginning early in life, and with a prolonged training-surgery interval, hippocampal lesions impair performance in the water maze task. Possible reasons for these findings are discussed in the context of the specific performance requirements of the water maze task.

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Section: Discussionmentioning

confidence: 57%

Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life

2005

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“…In trace eyeblink conditioning, the hippocampus is required for both acquisition (Solomon et al 1986;Moyer et al 1990;Beylin et al 2001) and retention of a recently acquired memory, but not of a remotely acquired one (Kim et al 1995;Takehara et al 2002Takehara et al , 2003a. These results suggest that the hippocampus is important for the early processes of memory (acquisition and consolidation), but the later processes (storage and retrieval) are mediated by other brain areas.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, this circuitry is reorganized after the CR has been completely acquired. Retention of a recently acquired CR is mediated mainly by the hippocampus (Kim et al 1995;Takehara et al 2002Takehara et al , 2003a and the cerebellum (Woodruff-Pak et al 1985;Takehara et al 2003a), but only marginally by the mPFC (Powell et al 2001;Takehara et al 2003a). Retention of a remotely acquired CR is mediated by the mPFC and the cerebellum (Takehara et al 2003a).…”

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confidence: 99%

NMDA receptor-dependent processes in the medial prefrontal cortex are important for acquisition and the early stage of consolidation during trace, but not delay eyeblink conditioning

Takehara‐Nishiuchi¹,

Kawahara²,

Kirino³

2005

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Permanent lesions in the medial prefrontal cortex (mPFC) affect acquisition of conditioned responses (CRs) during trace eyeblink conditioning and retention of remotely acquired CRs. To clarify further roles of the mPFC in this type of learning, we investigated the participation of the mPFC in mnemonic processes both during and after daily conditioning using local microinfusion of the GABA A receptor agonist muscimol or the NMDA receptor antagonist APV into the rat mPFC. Muscimol infusions into the mPFC before daily conditioning significantly retarded CR acquisition and reduced CR expression if applied after sufficient learning. APV infusion also impaired acquisition of CRs, but not expression of well-learned CRs. When infusions were made immediately after daily conditioning, acquisition of the CR was partially impaired in both the muscimol and APV infusion groups. In contrast, rats that received muscimol infusions 3 h after daily conditioning exhibited improvement in their CR performance comparable to that of the control group. Both the pre-and post-conditioning infusion of muscimol had no effect on acquisition in the delay paradigm. These results suggest that the mPFC participates in both acquisition of a CR and the early stage of consolidation of memory in trace, but not delay eyeblink conditioning by NMDA receptor-mediated operations.

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“…In these tasks, inactivation of the hippocampus impairs memory retrieval shortly after learning, but has no effect when performed weeks or months later (Kim and Fanselow 1992;Anagnostaras et al 1999;Clark et al 2002;Takehara et al 2002Takehara et al , 2003Maviel et al 2004;Ross and Eichenbaum 2006;Lesburgueres et al 2011;Tayler et al 2013; but see Clark et al 2005;Sutherland et al 2010). In addition, several regions of the neocortex become more important for memory retrieval with the passage of time.…”

Section: Animal Models Of Systems Consolidationmentioning

confidence: 99%

New methods for understanding systems consolidation

Tayler

Wiltgen

2013

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According to the standard model of systems consolidation (SMC), neocortical circuits are reactivated during the retrieval of declarative memories. This process initially requires the hippocampus. However, with the passage of time, neocortical circuits become strengthened and can eventually retrieve memory without input from the hippocampus. Although consistent with lesion data, these assumptions have been difficult to confirm experimentally. In the current review, we discuss recent methodological advances in behavioral neuroscience that are making it possible to test the basic assumptions of SMC for the first time. For example, new transgenic mice can be used to monitor the activity of individual neurons across the entire brain while optogenetic approaches provide precise control over the activity of these cells using light stimulation. These tools can be used to examine the reactivation of neocortical neurons during recent and remote memory retrieval and determine if this process requires the hippocampus.

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Time-limited role of the hippocampus in the memory for trace eyeblink conditioning in mice

Cited by 90 publications

References 40 publications

Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life

Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life

NMDA receptor-dependent processes in the medial prefrontal cortex are important for acquisition and the early stage of consolidation during trace, but not delay eyeblink conditioning

New methods for understanding systems consolidation

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