A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation

Swanson-Park, J.L; Coussens, Christine M.; Mason-Parker, Sara E.; Raymond, Clarke R.; Hargreaves, Eric L.; Dragunow, Michael; Cohen, Akiva S.; Abraham, Wickliffe C.

doi:10.1016/s0306-4522(99)00010-x

Cited by 167 publications

(149 citation statements)

References 45 publications

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“…The current data from this series of behavioral and electro-physiological experiments is supported by previous evidence for specific dopaminergic modulation of the direct pp (Empson and Heinemann, 1995;Huang and Kandel, 1995;Swanson-Park et al, 1999;Lisman, 1999, 2000;Li et al, 2003), and findings that have localized dense mesencephalic projections and high levels of DA receptors in dendritic layers of CA1 that receive afferent input via the pp (Frey et al, 1991;Bruinink and Bischoff, 1993;Goldsmith and Joyce, 1994;Carr and Sesack, 1996;Gasbarri et al, 1997). Thus, the observed deficits are assumed to be attributed to apomorphine acting on those receptors specifically.…”

Section: Discussionsupporting

confidence: 81%

“…Although the current data differ from inhibitory responses found in vitro (Otmakhova and Lisman, 1999), the observations are supported by previous data indicating that facilitation of LTP, specifically, the late proteinsynthesis dependent component of LTP in CA1 is dependent upon DA receptor activation (Frey et al, 1993;Huang and Kandel, 1995;Otmakhova and Lisman, 1996;Swanson-Park et al, 1999;Li et al, 2003). Differences may be due to the isolation of the hippocampal slice in vitro, in which the origins of the pathways are lost.…”

Section: Discussionsupporting

confidence: 77%

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The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

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Subregional analyses of the hippocampus have suggested a selective role for the CA1 subregion in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes. It remains unclear how the direct cortical projection to CA1 via the perforant path (pp) contributes to these CA1-dependent processes. It has been suggested that dopamine selectively modulates the pp projection to CA1 while having little to no effect on the Schaffer collateral (SC) projection to CA1. This series of behavioral and electro-physiological experiments takes advantage of this pharmacological dissociation to demonstrate that the direct pp inputs to CA1 are critical in CA1-dependent intermediate-term retention and retrieval function. Here we demonstrate that local infusion of the nonselective dopamine agonist, apomorphine (10, 15 μg), into the CA1 subregion of awake animals produces impairments in between-day retention and retrieval, sparing within-day encoding of a modified Hebb-Williams maze and contextual conditioning of fear. In contrast, apomorphine produces no deficits when infused into the CA3 subregion. To complement the behavioral analyses, electrophysiological data was collected. In anesthetized animals, local infusion of the same doses of apomorphine significantly modifies evoked responses in the distal dendrites of CA1 following angular bundle stimulation, but produces no significant effects in the more proximal dendritic layer following stimulation of the SC. These results support a modulatory role for dopamine in the EC-CA1, but not CA3-CA1 circuitry, and suggest the possibility of a more fundamental role for EC-CA1 synaptic transmission in terms of intermediate-term, but not short-term spatial memory.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionsupporting

confidence: 77%

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

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“…We found that at the Schaffer collateral (sc) inputs to CA1, activation of D1 dopamine receptors facilitated the induction of early LTP (Otmakhova and Lisman, 1996) and inhibited depotentiation of recently potentiated synapses (Otmakhova and Lisman, 1998). Other researchers confirmed these findings (Swanson-Park et al, 1999). Moreover, the CA1 region is not the only site of this action of dopamine.…”

Section: Dopamine Increases Nmda-dependent Ltp and Inhibits Depotentimentioning

confidence: 66%

“…6), a short pulse of dopamine would temporarily inhibit the pp input, removing CA1 from its most direct source of sensory information and switching its attention to CA3. At the same time, D1 dopamine receptors might facilitate LTP and inhibit depotentiation in the sc input to CA1 (Frey et al, 1993;Huang and Kandel, 1995;Lisman, 1996, 1998;Swanson-Park et al, 1999). This pattern would make sense from the following perspective: dopamine is released after novel, salient, or reinforcement-relevant stimuli (see above).…”

Section: Other Possible Functions Of Ca1: Switching An Input Sourcementioning

confidence: 99%

Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine

2001

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ABSTRACT:In order to understand how the molecular or cellular defects that underlie a disease of the nervous system lead to the observable symptoms, it is necessary to develop a large-scale neural model. Such a model must specify how specific molecular processes contribute to neuronal function, how neurons contribute to network function, and how networks interact to produce behavior. This is a challenging undertaking, but some limited progress has been made in understanding the memory functions of the hippocampus with this degree of detail. There is increasing evidence that the hippocampus has a special role in the learning of sequences and the linkage of specific memories to context. In the first part of this paper, we review a model (the SOCRATIC model) that describes how the dentate and CA3 hippocampal regions could store and recall memory sequences in context. A major line of evidence for sequence recall is the "phase precession" of hippocampal place cells. In the second part of the paper, we review the evidence for theta-gamma phase coding. According to a framework that incorporates this form of coding, the phase precession is interpreted as cued recall of a discrete sequence of items from long-term memory. The third part of the paper deals with the issue of how the hippocampus could learn memory sequences. We show that if multiple items can be active within a theta cycle through the action of a short-term "buffer," NMDA-dependent plasticity can lead to the learning of sequences presented at realistic item separation intervals. The evidence for such a buffer function is reviewed. An important underlying issue is whether the hippocampal circuitry is configured differently for learning and recall. We argue that there are indeed separate states for learning and recall, but that both involve theta oscillations, albeit in possibly different forms. This raises the question of how neuromodulatory input might switch the hippocampus between learning and recall states and more generally how different neuromodulatory inputs reconfigure the hippocampus for different functions. In the fifth part of this paper we review our studies of dopamine and dopamine/NMDA interactions in the control of synaptic function. Our results show that dopamine dramatically reduces the direct cortical input to CA1 (the perforant path input), while having little effect on the input from CA3. In order to interpret the functional consequences of this pathway-specific modulation, it is necessary to understand the function of CA1 and the role of dopaminergic input from the ventral tegmental area (VTA). In the sixth part of this paper we consider several possibilities and address the issue of how dopamine hyperfunction or NMDA hypofunction, abnormalities that may underlie schizophrenia, might lead to the symptoms of the disease. Relevant to this issue is the demonstrated role of the hippocampus in novelty detection, a function that is likely to depend on sequence recall by the hippocampus. Novelty signals are generated when reality does not match ...

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“…Several studies have shown that generation of the late-phase of CA1 LTP is critically dependent on activation of D1/D5 dopamine receptors, both in vitro and in vivo (Frey et al 1990;Swanson-Park et al 1999). Whether activation of D1/D5 receptors is sufficient to induce late-phase LTP is more debatable (Huang & Kandel 1995;Swanson-Park et al 1999), and it is likely that late-phase LTP requires coactivation of both dopamine and NMDA receptors. Because D1/D5 receptors couple to G s -proteins, one such coincidence detector could be Type I adenylyl cyclase, which is activated by both calcium and G s -proteins.…”

Section: How Long Will Ltp Persist?mentioning

confidence: 99%

How long will long-term potentiation last?

Abraham

2003

Phil. Trans. R. Soc. Lond. B

233

165

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The paramount feature of long-term potentiation (LTP) as a memory mechanism is its characteristic persistence over time. Although the basic phenomenology of LTP persistence was established 30 years ago, new insights have emerged recently about the extent of LTP persistence and its regulation by activity and experience. Thus, it is now evident that LTP, at least in the dentate gyrus, can either be decremental, lasting from hours to weeks, or stable, lasting months or longer. Although mechanisms engaged during the induction of LTP regulate its subsequent persistence, the maintenance of LTP is also governed by activity patterns post-induction, whether induced experimentally or generated by experience. These new findings establish dentate gyrus LTP as a useful model system for studying the mechanisms governing the induction, maintenance and interference with long-term memory, including very long-term memory lasting months or longer. The challenge is to study LTP persistence in other brain areas, and to relate, if possible, the properties and regulation of LTP maintenance to these same properties of the information that is actually stored in those regions.Keywords: long-term potentiation; hippocampus; maintenance mechanisms; enriched environment; neurogenesis; metaplasticitySince the pioneering studies performed 30 years ago by Tim Bliss, Terje Lømo and Tony Gardner-Medwin (Bliss & Lømo 1973;Bliss & Gardner-Medwin 1973), LTP has generated enormous interest as a potential memory mechanism. This is because LTP exhibits numerous properties expected of an associative memory mechanism, such as rapid induction, input specificity, associative interactions, persistence, and dependence on correlated preand postsynaptic activity. The close similarity between these features and those of the learning rule of Hebb (1949) has added lustre to the LTP phenomenon. In addition, there is important yet complex regulation of LTP by prior synaptic activity (metaplasticity), neighbouring afferents (e.g. synaptic tagging), and state variables such as levels of stress hormones and activity in neuromodulatory transmitter systems (see Martin et al. (2000) for a review of these properties of LTP). It can be argued, however, that among all these intriguing and important characteristics, the paramount feature that defines LTP as a potential memory mechanism is its persistence over time. Thus, although short-lasting frequency potentiation of synaptic potentials was described in the hippocampus many years ago, it was not until the discovery of LTP that researchers seriously considered that a model system for studying synaptic mechanisms of mammalian memory had been established. It is curious, therefore, that despite the fundamental importance of LTP maintenance over days and weeks, relatively few studies have addressed its mechanisms and regulation. The purpose of this review is to summarize the data from experiments charting how long LTP can last, and then to address the factors that regulate how long LTP will in fact persist under various conditi...

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A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation

Cited by 167 publications

References 45 publications

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine

How long will long-term potentiation last?

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