Both non-NMDA and NMDA glutamate receptors are necessary for memory consolidation in the day-old chick

doi:10.1016/S0163-1047(05)80056-1

Behavioral and Neural Biology

Volume 62, Issue 1, July 1994, Pages 33-40

https://doi.org/10.1016/S0163-1047(05)80056-1 Get rights and content

Day-old chicks (black Australorp-white Leghorn)trained to avoid an aversive stimulus will usually retain memory for this event indefinitely. The passive avoidance task used involves a period of pretraining where chicks peck freely at two differently colored glass beads, a single training trial where one of the beads is coated in a chemical aversant eliciting typical disgust reactions from the chicks, and a test trial where both beads are presented dry, and discrimination memory is demonstrated by avoidance of the previously aversive bead with continued pecking of the nonaversive bead. Intracranial administration of a N-methyl-d-aspartate glutamate receptor antagonist (50 μM 2-amino-5-phosphopentanoate) immediately after or prior to learning, or a non-N-methyl-d-aspartate glutamate receptor antagonist (100 μM 6,7-dinitro-quinoxaline-2,3-dione) between 10 and 25 min after learning, resulted in amnesia for this taks at 80 to 90 min post-training. These data indicate that processes dependent on N-methyl-d-aspartate and non-N-methyl-d-aspartate glutamate receptor activation are necessary for memory consolidation of a passive avoidance task in the day-old chick. Since these agents must be administered during the earlier stages of memory formation to cause amnesia, the receptors are probably activated close to the time of learning. The delayed effect of these antagonists, however, suggests that memory is independent of these receptors until quite late in the memory consolidation process.

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Cited by (72)

Memory reacquisition deficit: Chicks fail to relearn pharmacologically disrupted associative response
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It is generally assumed that if memory is disrupted by pharmacological inhibitors during its consolidation, it can be later acquired afresh. In our experiments, we trained day-old chicks in a one-trial passive avoidance task and interfered with memory formation using protein synthesis inhibitor anisomycin or NMDA receptor antagonist MK-801. Second training was then given to amnestic animals with either the same conditioning stimulus (retraining) or a new one (novel training). Retraining with the same stimulus failed to produce efficient memory at all the examined between-training and training-to-test intervals, while a new conditioned stimulus was learned successfully. We suggest that this memory reacquisition deficit may result from the failure of associative memory co-allocation mechanisms.
Effect of acute lipopolysaccharide-induced inflammation in intracerebroventricular-streptozotocin injected rats
2016, Neuropharmacology
Lipopolysaccharide (LPS) is often used to investigate the exacerbatory effects of an immune-related challenge in transgenic models of various neurodegenerative diseases. However, the effects of this inflammatory challenge in an insulin resistant brain state, as seen in diabetes mellitus, a major risk factor for both vascular dementia (VaD) and Alzheimer's disease (AD), is not as well characterized. We investigated the effects of an LPS-induced inflammatory challenge on behavioral and biological parameters following intracerebroventricular (ICV) injection of streptozotocin (STZ) in male Sprague–Dawley rats. Subjects received a one-time bilateral ICV infusion of STZ (25 mg/mL, 8 μL per ventricle) or ACSF. One week following ICV infusions, LPS (1 mg/mL, i.p.) or saline was administered to activate the immune system. Behavioral testing began on the 22nd day following STZ-ICV infusion, utilizing the open field and Morris water maze (MWM) tasks. Proteins related to immune function, learning and memory, synaptic plasticity, and key histopathological markers observed in VaD and AD were evaluated. The addition of an LPS-induced immune challenge partially attenuated spatial learning and memory deficits in the MWM in STZ-ICV injected animals. Additionally, LPS administration to STZ-treated animals partially mitigated alterations observed in several protein levels in STZ-ICV alone, including NR2A, GABA_B1, and β-amyloid oligomers. These results suggest that an acute LPS-inflammatory response has a modest protective effect against some of the spatial learning and memory deficits and protein alterations associated with STZ-ICV induction of an insulin resistant brain state.
Effects of CA1 glutamatergic systems upon memory impairments in cholestatic rats
2013, Behavioural Brain Research
Citation Excerpt :
Thus, NMDA receptors are known to be implicated in some mechanisms of synaptic plasticity such as long-term potentiation (LTP), spatial, and non-spatial forms of learning in the hippocampus and other brain regions [42,87,88]. In support of our findings, cumulative evidence have substantiated that NMDA improves [21,29,31,37,89–91], while NMDA antagonists impair learning and memory in a variety of tasks [92–95]. There are also some solid experimental evidences showing that NMDA activity modulates the synaptic plasticity and facilitates long-term potentiation in various areas of the brain [21,23,32,79,80].
Bile duct ligation (BDL) is shown to induce cholestasis-related liver function impairments as well as consequent cognitive dysfunctions (i.e. impaired learning and memory formation). Glutamatergic neurotransmission plays an important role in hippocampal modulation of learning and memory function. The present study aimed to investigate the possible involvement of dorsal hippocampal (CA1) glutamatergic systems upon cholestasis-induced amnesia.
Cholestasis was induced in male Wistar rats through double-ligation of the main bile duct (at two points) and transection of the interposed segment. Step-through passive avoidance test was employed to examine rats’ learning and memory function. All drugs were injected into CA1 region of the hippocampus.
our results indicated a decrease in memory retrieval following cholestasis (11, 17 and 24 days post BDL). Only subthreshold doses of N-methyl-d-aspartate (NMDA; 0.125 and 0.25 μg/μl) but not its effective dose (0.5 μg/μl), restored the cholestasis-induced amnesia in step-through passive avoidance test, 11, 17 and 24 days post BDL. This effect was blocked by the subthreshold dose of D-[1]-2-amino-7-phosphonoheptanoic acid (D-AP7, NMDA receptor antagonist; 0.0625 μg/μl, intra-CA1) at 0.125 μg/μl and 0.25 μg/μl doses of NMDA. Moreover, our data revealed that only effective doses of D-AP7 (0.125 and 0.25 μg/μl, intra-CA1) potentiate memory impairments in 11 days after BDL. It was noted that none of applied drugs/doses exerted an effect on memory acquisition and locomotors activity, 10 and 12 days post laparotomy, respectively.
Our findings suggest the potential involvement of CA1 glutamatergic system(s) in cholestasis-induced memory deficits.
Involvement of Glutamate in Learning and Memory
2013, Identification of Neural Markers Accompanying Memory
Since its discovery in the early 1950s, glutamate has been involved in fundamental functions, including neuronal plasticity, neurotoxicity, development, learning and memory. Describing our current knowledge of glutamate role in learning and memory processes would be impossible in few pages. Therefore, the aim of this chapter is to provide a brief overview of findings available to date, summarizing the main characteristic of glutamate receptors and their involvement in learning and memory. Moreover, we briefly describe the involvement of glutamate in hippocampal formation and, in particular, its role in learning and memory, including addiction as the persistence of maladaptive memory, and nervous diseases.
The role of intracellular calcium stores in synaptic plasticity and memory consolidation
2013, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
It is therefore difficult to be conclusive regarding the activation source of SK channels in this avian model of memory from the present correlational evidence. While the range of effective times of administration for SK channel inhibition is broadly shared by mGluR1 and IP3R antagonists (Baker et al., 2008, 2011a), this is inconsistent with the narrow time frame of susceptibility to NMDAR inhibition (Rickard et al., 1994b). The common window of effective administration times is consistent with IP3Rs as a source of intracellular Ca2+ for SK channel activation.
Memory processing requires tightly controlled signalling cascades, many of which are dependent upon intracellular calcium (Ca²⁺). Despite this, most work investigating calcium signalling in memory formation has focused on plasma membrane channels and extracellular sources of Ca²⁺. The intracellular Ca²⁺ release channels, ryanodine receptors (RyRs) and inositol (1,4,5)-trisphosphate receptors (IP₃Rs) have a significant capacity to regulate intracellular Ca²⁺ signalling. Evidence at both cellular and behavioural levels implicates both RyRs and IP₃Rs in synaptic plasticity and memory formation. Pharmacobehavioural experiments using young chicks trained on a single-trial discrimination avoidance task have been particularly useful by demonstrating that RyRs and IP₃Rs have distinct roles in memory formation. RyR-dependent Ca²⁺ release appears to aid the consolidation of labile memory into a persistent long-term memory trace. In contrast, IP₃Rs are required during long-term memory. This review discusses various functions for RyRs and IP₃Rs in memory processing, including neuro- and glio-transmitter release, dendritic spine remodelling, facilitating vasodilation, and the regulation of gene transcription and dendritic excitability. Altered Ca²⁺ release from intracellular stores also has significant implications for neurodegenerative conditions.
Piracetam, an AMPAkine drug, facilitates memory consolidation in the day-old chick
2012, Pharmacology Biochemistry and Behavior
Citation Excerpt :
AMPA receptors are involved in long-term potentiation (LTP), which is believed to be the key neurophysiological process underlying the formation and consolidation of memory (e.g. Lynch, 1998). It has been previously shown that inhibition of AMPA receptor activity results in memory deficit (e.g. Rickard et al., 1994). The facilitative effect of various AMPAkines on memory functioning has been explored in both animals and humans.
Piracetam is an AMPAkine drug that may have a range of different mechanisms at the cellular level, and which has been shown to facilitate memory, amongst its other effects. This series of experiments demonstrated that a 10 mg/kg dose of piracetam facilitated memory consolidation in the day-old chick when injected from immediately until 120 min after weak training (i.e. using a 20% v/v concentration of methyl anthranilate) with the passive avoidance learning task. Administration of piracetam immediately after training led to memory facilitation which lasted for up to 24 h following training. This dose of the AMPAkine was not shown to facilitate memory reconsolidation. These findings support the contention that application of the AMPAkine piracetam facilitates memory using a weak training task, and extend the range of actions previously noted with NMDA-related agents to those which also facilitate the AMPA receptor.

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¹: Research was supported by an Australian Research Council grant.

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Behavioral and Neural Biology

References (29)

Excitatory amino acids and memory—Evidence from research on Alzhemier's disease and behavioral pharmacology

Neuroscience and Biobehavioral Reviews

NMDA receptors: Their role in long-term potentiation

Trends in Neuroscience

Forebrain noradrenaline concentration following weakly reinforced training

Pharmacology, Biochemistry, and Behaviour

Effects of social isolation on memory formation

Behavioral and Neural Biology

Late posttraining memory processing by entorhinal cortex—Involvement of NMDA andGABAergic receptors

Pharmacology Biochemistry and Behavior

Psychobiology of memory: Towards a model of memory formation

Biobehavioral Reviews

Dual action of cycloheximide on memory formation in day-old chicks

Behavioural Brain Research

Amnesia by post-training infusion of glutamate receptor antagonists into the amygdala, hippocampus, and entorhinal cortex

Behavioral and Neural Biology

How chicks make memories—The cellular cascade from c-fos to dendritic remodelling

Trends in Neurosciences

Classical conditioning selectively increases AMPA receptor binding in rabbit hippocampus

Brain Research

Effects of the novel NMDA antagonist, NPC 12626, on long-term potentiation, learning and memory

Brain Research

Effects of the NMDA antagonists CPP and MK-801 on radial arm maze performance in rats

Pharmacology, Biochemistry and Behaviour

Memory formation in day-old chicks requires NMDA but not non-NMDA glutamae receptors

European Journal of Neuroscience

Temporally distinct pre-and postsynaptic mechanisms maintain long-term potentiation

Nature

Cited by (72)

Memory reacquisition deficit: Chicks fail to relearn pharmacologically disrupted associative response

Effect of acute lipopolysaccharide-induced inflammation in intracerebroventricular-streptozotocin injected rats

Effects of CA1 glutamatergic systems upon memory impairments in cholestatic rats

Involvement of Glutamate in Learning and Memory

The role of intracellular calcium stores in synaptic plasticity and memory consolidation

Piracetam, an AMPAkine drug, facilitates memory consolidation in the day-old chick