Amino acid neurotransmitter release and learning: a study of visual imprinting

doi:10.1016/j.neuroscience.2004.03.046

Neuroscience

Volume 126, Issue 2, 2004, Pages 249-256

https://doi.org/10.1016/j.neuroscience.2004.03.046 Get rights and content

Abstract

The intermediate and medial part of the hyperstriatum ventrale (IMHV) is an area of the domestic chick forebrain that stores information acquired through the learning process of imprinting. The effects of visual imprinting on the release of the amino acids aspartate, arginine, citrulline, γ-aminobutyric acid (GABA), glutamate, glycine and taurine from the left and right IMHVs in vitro were measured at 3.5, 10 and 24 h after training. Chicks were exposed to an imprinting stimulus for 1 h, their preferences measured 10 min afterward and a preference score calculated as a measure of the strength of learning. Potassium stimulation was used to evoke amino acid release from the IMHVs of trained and untrained chicks in the presence and absence of extracellular Ca²⁺. Ca²⁺-dependent, K⁺-evoked release of glutamate was significantly (34.4%) higher in trained than in untrained chicks. This effect was not influenced by time after training or by side (left or right IMHV). Training influenced the evoked release of GABA and taurine from the left IMHV at both 3.5 and 10 h. The training effects at the two times were statistically homogeneous so data (≤10 h group) were combined for each amino acid respectively. For this ≤10 h group, evoked release increased significantly with preference score. In contrast, for the 24 h group, evoked release of GABA and taurine was not significantly correlated with preference score. There were no significant correlations between preference score and GABA or taurine release in the right IMHV at any time, nor in the absence of extracellular calcium. No significant effects of training condition, time or side were observed for any other amino acid in the study.

The present findings suggest that soon after chicks have been exposed to an imprinting stimulus glutamatergic excitatory transmission in IMHV is enhanced, and remains enhanced for at least 24 h. In contrast, the learning-related elevations in taurine and GABA release are not sustained over this period. The change in GABA release may reflect a transient increase in inhibitory transmission in the left IMHV.

Section snippets

Behavioural training

Domestic chicks (Gallus gallus domesticus; Ross 1 breed; Grampian Country Chickens Ltd., Stanton, UK) were hatched and reared in darkness and transferred to individual compartments in a holding incubator at 34 °C. When they were 18–24 h old, chicks were allocated at random to be trained or remain untrained. The experiment was replicated on each of 10 hatches of chicks.

Each chick was placed in a running wheel in darkness and then trained by being exposed to one of two imprinting stimuli for 60

Behaviour

The overall mean value of training approach was 192.5±23.5 metres (mean±S.E.M., n=60 chicks); the data were pooled because training approach was not affected significantly by Training Condition, Time or Training Stimulus and an ANOVA revealed no significant interactions between any of these factors. The mean approach activity during the preference test for all chicks combined was 13.6±1.5 metres (n=60); there were no significant main effects or interactions. The mean preference scores of good

Discussion

When measured within the first 10 h after imprinting training, potassium-stimulated release of GABA and taurine from the left IMHV in the presence of calcium ions was significantly and positively correlated with preference score: the higher the preference score the greater was the release of these amino acids in response to the potassium challenge. That is, the more strongly imprinted chicks released significantly more GABA and taurine from the left IMHV in response to potassium stimulation

Acknowledgements

Supported by the BBSRC and the Leverhulme Trust.

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Subtype-selective contribution of muscarinic acetylcholine receptors for filial imprinting in newly-hatched domestic chicks
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The bilateral ablation of the IMM causes anterograde amnesia [12]. During imprinting training in the IMM, three neurotransmitters, i.e., glutamate, GABA, acetylcholine, have been reported to be released from IMM neurons [13,14]. In the released neurotransmitters, we have studied the roles of GABA and acetylcholine in imprinting.
Muscarinic acetylcholine receptors (mAChRs) play an important role in many brain functions. Our previous study revealed that the injection of mAChRs antagonist scopolamine into the intermediate medial mesopallium (IMM) region, which is critical for filial imprinting, impairs memory formation. In avian brains, four mAChR subtypes have been identified (M₂, M₃, M₄ and M₅). M₃ and M₅ receptors increase the excitability of neurons, whereas M₂ and M₄ receptors reduce the excitability. Because the scopolamine blocks all subtypes, the previous study did not identify which subtype contributes to the memory formation. By injecting several types of mAChR antagonists into the IMM, in this study we determined which mAChR subtype plays a critical role in imprinting. First, the effects of antagonists on the excitatory receptor subtypes M₃ and M₅ were examined. Injection of the M₃ antagonist (DAU5884) at 20 mM or the M₅ antagonist (ML381) at 2 mM impaired imprinting. Considering the pKi value of DAU5884, the impairment seems to be caused by DAU5884 binding to M₃ and/or M₄ receptors. Second, the effect of antagonists on the inhibitory receptor subtype M₂ was examined. The results showed that the M₂ antagonist (AQ-RA741) impaired imprinting at a concentration of 20 mM. Considering the pKi value of AQ-RA741, the impairment seems to be caused by AQ-RA741 binding to M₂ and/or M_4. The findings of this study suggests that the excitatory receptor subtypes M₃ and M₅ and the inhibitory receptor subtype M₂ and/or M₄ cooperate to achieve the appropriate balance of acetylcholine signaling to execute imprinting.
Neural mechanisms of imprinting
2021, Encyclopedia of Behavioral Neuroscience: Second Edition
Filial imprinting is a process by which young animals restrict their social preferences to stimuli through being exposed to these stimuli. The intermediate and medial mesopallium (IMM) of the chick forebrain stores information about a visual imprinting stimulus. Learning-related changes including synaptic modification occur in the IMM, which together with another region (S′) subserves recognition of an imprinting stimulus. Sleep is critical for imprinting and its associated neuronal activity in the IMM. Imprinting occurs during a sensitive period, which can be modified pharmacologically, and acts in conjunction with predispositions that are manifest as predilections for certain animal-like features. The neural mechanisms of filial imprinting and these related processes are discussed.
Blockade of muscarinic acetylcholine receptor by scopolamine impairs the memory formation of filial imprinting in domestic chicks (Gallus Gallus domesticus)
2020, Behavioural Brain Research
Citation Excerpt :
Therefore, it is considered that the IMM is necessary for the early phase of memory formation and that the imprinted memory is subsequently transferred to other brain regions such as intermediate hyperpallium apicale (IMHA) [4]. During the early phase of memory formation, several neurotransmitters increase in the IMM, e.g., glutamate, taurine, GABA, and acetylcholine [5,6]. With regard to GABA, we recently found that the balance of two types of GABA receptor (GABA-A and GABA-B receptors) expression in the chick brain developmentally changed, which determines whether the chicks are able to be imprinted or not [7].
Filial imprinting in precocial birds is a useful model for studying memory formation in early learning. The intermediate medial mesopallium (IMM) in the dorsal telencephalon is one of the critical brain regions where the releases of several neurotransmitters increase after the start of imprinting training. Among the increased neurotransmitters, the role of acetylcholine in imprinting has remained unclear. Acetylcholine in the mammalian brain plays an important role in encoding new memories. The muscarinic acetylcholine receptor subtype 1 (M₁ receptor) and subtype 3 (M₃ receptor) in the hippocampus and cortex of mammalian brain have been shown to be necessary for memory encoding. In this study, we examined whether the imprinting acquisition in chick can be impaired by injecting muscarinic acetylcholine receptor (mAChR) antagonist scopolamine into the bilateral IMM. We show that the injection of scopolamine decreased the preference for the imprinting object in the test, but did not affect the number of approaches to the imprinting object during training. Immunoblotting and immunohistochemistry revealed that M₃ receptors were expressed in the IMM. Our data suggest that acetylcholine is involved in the memory formation of imprinting through M₃ receptors in the IMM. The scopolamine-injected chicks may be useful as an animal model for dementia such as Alzheimer’s disease.
Memory-related brain lateralisation in birds and humans
2015, Neuroscience and Biobehavioral Reviews
Visual imprinting in chicks and song learning in songbirds are prominent model systems for the study of the neural mechanisms of memory. In both systems, neural lateralisation has been found to be involved in memory formation. Although many processes in the human brain are lateralised – spatial memory and musical processing involves mostly right hemisphere dominance, whilst language is mostly left hemisphere dominant – it is unclear what the function of lateralisation is. It might enhance brain capacity, make processing more efficient, or prevent occurrence of conflicting signals. In both avian paradigms we find memory-related lateralisation. We will discuss avian lateralisation findings and propose that birds provide a strong model for studying neural mechanisms of memory-related lateralisation.
Molecular mechanisms of memory in imprinting
2015, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
Potassium-stimulated, calcium-dependent release of GABA and taurine, whilst significantly correlated with strength of learning up to 11 h after the start of training, ceased to be so at 25 h. In contrast, release of glutamate in trained chicks persisted up to this time (McCabe et al., 2001; Meredith et al., 2004). At the early and intermediate stages after training, the amount of clathrin may not be rate-limiting for vesicle recycling.
Converging evidence implicates the intermediate and medial mesopallium (IMM) of the domestic chick forebrain in memory for a visual imprinting stimulus. During and after imprinting training, neuronal responsiveness in the IMM to the familiar stimulus exhibits a distinct temporal profile, suggesting several memory phases. We discuss the temporal progression of learning-related biochemical changes in the IMM, relative to the start of this electrophysiological profile. c-fos gene expression increases <15 min after training onset, followed by a learning-related increase in Fos expression, in neurons immunopositive for GABA, taurine and parvalbumin (not calbindin). Approximately simultaneously or shortly after, there are increases in phosphorylation level of glutamate (AMPA) receptor subunits and in releasable neurotransmitter pools of GABA and taurine. Later, the mean area of spine synapse post-synaptic densities, N-methyl-d-aspartate receptor number and phosphorylation level of further synaptic proteins are elevated. After ∼15 h, learning-related changes in amounts of several synaptic proteins are observed. The results indicate progression from transient/labile to trophic synaptic modification, culminating in stable recognition memory.
Mitochondrial proteins, learning and memory: Biochemical specialization of a memory system
2011, Neuroscience
The enzyme cytochrome c oxidase is a mitochondrial protein complex that plays a crucial role in oxidative metabolism. In the present study we show that amounts of two of its protein subunits (cytochrome c oxidase subunit I [CO-I] and II [CO-II]) are influenced by both learning-independent and learning-dependent factors. Converging evidence has consistently implicated the left intermediate medial mesopallium (IMM) in the chick brain as a memory store for the learning process of visual imprinting. This form of learning proceeds very shortly after chicks have been hatched. In the left IMM, but not in three other brain regions studied, amounts of CO-I and CO-II co-varied: the correlation between them was highly significant. This relationship did not depend on learning. However, learning influenced the amounts of both proteins, but did so only in the left IMM. In this region, amounts of each protein increased with the strength of learning. These findings raise the possibility that the molecular mechanisms involved in the coordinated assembly of cytochrome c oxidase are precociously developed in the left IMM compared to the other regions studied. This precocious development may enable the region to respond efficiently to the oxidative demands made by the changes in synaptic connectivity that underlie memory formation and would allow the left IMM to function as a storage site within hours after hatching.

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Amino acid neurotransmitter release and learning: a study of visual imprinting

Abstract

Section snippets

Behavioural training

Behaviour

Discussion

Acknowledgements

Brain Res

Neuroscience

Anim Behav

Anim Behav

Neurobiol Learn Mem

Neuropharmacology

Trends Neurosci

Neuropsychologia

Behav Brain Res

Curr Opin Cell Biol

Neuroscience

Brain Res

Neuroscience

Behav Brain Res

Neuroscience

Neuroscience

Brain Res

Anim Behav

The characteristics and context of imprinting

Biol Rev

Mechanisms of avian imprintingA review

Biol Rev

Local circuitry in the IMHV of the domestic chick (Gallus domesticus)

Proc R Soc B

Connections of the IMHV in the domestic chick Gallus domesticus

Proc R Soc B

ImprintingAn electron microscopic study of chick hyperstriatum ventrale

Exp Brain Res

Robust tests for the equality of variances

J Am Stat Assoc

Learning-related alterations in the visual responsiveness of neurons in a memory system of the chick brain

Eur J Neurosci

Passive avoidance training and recall are associated with increased glutamate levels in the intermediate medial hyperstriatum ventrale of the day-old chick

Neural Plast