Learning-induced lateralized activation of the MAPK/ERK cascade in identified neurons of the food-aversion network in the mollusk Helix lucorum

Kharchenko, O. A.; Grinkevich, Vera; Vorobiova, O. V.; Grinkevich, L. N.

doi:10.1016/j.nlm.2010.05.002

Cited by 17 publications

(14 citation statements)

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“…These effects only differ in their magnitude and duration (Abrams et al, 1991; Grinkevich, 1994; Antonov et al, 2001). Moreover, our recent findings (Kharchenko et al, 2010) support the idea of a significant role of sensitization in the molecular processes underlying withdrawal reflex formation. We have shown asymmetrical activation of MAPK/ERK in RPa(2/3) neurons not only after learning but also after incubation in serotonin, the neurotransmitter which mediates the effect of the US and stimulates sensitization.…”

Section: Discussionsupporting

confidence: 81%

“…We aimed at understanding whether histone H3 acetylation is induced in RPa(2/3) and LPa(2/3) command neurons after learning and whether it is MAPK/ERK-dependent. We analyzed if, consistently with MAPK/ERK activation observed in our previous work (Kharchenko et al, 2010), learning-dependent induction of histone H3 acetylation is also asymmetrical between the left and right command neurons. Our results show that food aversion learning in Helix induces a significant learning-dependent increase in histone H3 acetylation in command neurons of the right parietal ganglion RPa(2/3) but not in the symmetrical command neurons of the left parietal ganglion LPa(2/3).…”

Section: Introductionsupporting

confidence: 55%

“…Balaban (1979) reported that RPa(2/3) and LPa(2/3) neurons are responsible for producing contractions of ipsilateral body walls so that they may not be involved in the production of bilateral movements of the foot, which are mediated by ipsilateral populations of motor neurons. We focused on left and right command neurons and showed that serotonin-dependent MAPK/ERK activation is involved in the formation of the withdrawal reflex; moreover we found that following learning, there is an asymmetry of MAPK/ERK activation in the left and right command neurons, which could result in the lateralization of molecular memory processes (Kharchenko et al, 2010). Specifically, we found that after food aversion learning phospho-ERK levels increased significantly in RPa(2/3) command neurons but no increase was found in LPa(2/3) command neurons.…”

Section: Introductionmentioning

confidence: 99%

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Histone H3 Acetylation is Asymmetrically Induced Upon Learning in Identified Neurons of the Food Aversion Network in the Mollusk Helix Lucorum

Danilova¹,

Kharchenko²,

Шевченко³

et al. 2010

Front. Behav. Neurosci.

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Regulation of gene expression is an essential step during long-term memory formation. Recently, the involvement of DNA-binding transcription factors and chromatin remodeling in synaptic plasticity have been intensively studied. The process of learning was shown to be associated with chromatin remodeling through histone modifications such as acetylation and phosphorylation. We have previously shown that the MAPK/ERK (mitogen-activated protein kinase/extracellular signal-regulated kinase) regulatory cascade plays a key role in the food aversion conditioning in the mollusk Helix. Specifically, command neurons of withdrawal behavior exhibit a learning-dependent asymmetry (left–right) in MAPK/ERK activation. Here, we expanded our molecular studies by focusing on a potential MAPK/ERK target – histone H3. We studied whether there is a learning-induced MAPK/ERK-dependent acetylation of histone H3 in command neurons RPa(2/3) and LPa(2/3) of the right and left parietal ganglia and whether it is asymmetrical. We found a significant learning-dependent increase in histone H3 acetylation in RPa(2/3) neurons but not in LPa(2/3) neurons. Such an increase in right command neurons depended on MAPK/ERK activation and correlated with a lateralized avoidance movement to the right visible 48 h after training. The molecular changes found in a selective set of neurons could thus represent a lateralized memory process, which may lead to consistent turning in one direction when avoiding a food that has been paired with an aversive stimulus.

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Section: Discussionsupporting

confidence: 81%

Section: Introductionsupporting

confidence: 55%

Section: Introductionmentioning

confidence: 99%

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Histone H3 Acetylation is Asymmetrically Induced Upon Learning in Identified Neurons of the Food Aversion Network in the Mollusk Helix Lucorum

Danilova¹,

Kharchenko²,

Шевченко³

et al. 2010

Front. Behav. Neurosci.

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“…Besides this, during formation of avoidance reflexes, including food aversion, an excitability and the amount of bound calcium changes in command neurons [27], [28], [29], [30]. Previously we found that in the case of food avoidance learning of adult Helix , following 15 minutes training, there is a significant activation of MAPK/ERK kinase and histone H3 acetylation in command neurons of the left, but not right parietal ganglion [21], [23]. The observed changes in histone H3 acetylation level in identified command neurons of parietal ganglia were less pronounced compared to our current study (where we investigated total subesaphoegal complex).…”

Section: Discussionmentioning

confidence: 99%

“…We hypothesized that immaturity of the serotonin signal transduction underlies the inability of juvenile mollusks Helix to form long-term types of avoidance behavior [13]. Previously, we showed that the MAPK/ERK regulatory cascade mediates serotonin signaling and plays the key role in the formation of the food aversion reflex in Helix [13], [20], [21], [22]. Recently we found that upon learning, in adult Helix, there is a MAPK/ERK dependent asymmetric increase of histone H3 acetylation in the command neurons of the right parietal ganglia RPa(2/3), but not in the symmetrical command neurons of the left parietal ganglia LPa(2/3) [23].…”

Section: Introductionmentioning

confidence: 99%

Failure of Long-Term Memory Formation in Juvenile Snails Is Determined by Acetylation Status of Histone H3 and Can Be Improved by NaB Treatment

Danilova

Grinkevich

2012

PLoS ONE

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BackgroundAnimals’ capacities for different forms of learning do not mature simultaneously during ontogenesis but the molecular mechanisms behind the delayed development of specific types of memory are not fully understood. Mollusks are considered to be among the best models to study memory formation at the molecular level. Chromatin remodeling in developmental processes, as well as in long-term memory formation, was recently shown to play a major role. Histone acetylation is a key process in the chromatin remodeling and is regulated through the signaling cascades, for example MAPK/ERK. Previously, we found that MAPK/ERK is a key pathway in the formation of the food aversion reflex in Helix. Pretreatment with upstream ERK kinase inhibitor PD98059 prevented food avoidance learning in adult Helix. In contrast to adult snails, juveniles possess immature plasticity mechanisms of the avoidance reflex until the age of 2–3 months while the MAPK/ERK cascade is not activated after aversive learning. In the present study, we focused on the potential MAPK/ERK target - histone H3.Methodology/Principal FindingsHere we found that a significant increase in histone H3 acetylation occurs in adult animals after learning, whereas no corresponding increase was observed in juveniles. The acetylation of histone H3 is regulated by ERK kinase, since the upstream ERK kinase inhibitor PD98059 prevented the increase of histone H3 acetylation upon learning. We found that the injection of histone deacetylase inhibitor sodium butyrate (NaB) prior to training led to induction in histone H3 acetylation and significantly ameliorated long-term memory formation in juvenile snails.Conclusions/SignificanceThus, MAPK/ERK-dependent histone H3 acetylation plays an essential role in the formation of food aversion in Helix. Dysfunction of the MAPK/ERK dependent histone H3 acetylation might determine the deficiency of avoidance behavior and long-term plasticity in juvenile animals. Stimulation of histone H3 acetylation in juvenile animals by NaB promoted avoidance plasticity.

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The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization

Jordan

2019

Hippocampus

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The left and right rodent hippocampi exhibit striking lateralization in some of the very neural substrates considered to be critical for hippocampal cognitive function. Despite this, there is an overwhelming lack of consideration for hemispheric differences in studies of the rodent hippocampus. Asymmetries identified so far suggest that a bilateral model of the hippocampus will be essential for an understanding of this brain region, and perhaps of the brain more widely. Although hypotheses have been proposed to explain how the left and right hippocampi contribute to behavior and cognition, these hypotheses have either been refuted by more recent studies or have been limited in the scope of data they explain. Here, I will first review data on human and rodent hippocampal lateralization. The implications of these data suggest that considering the hippocampus as a bilateral structure with functional lateralization will be critical moving forward in understanding the function and mechanisms of this brain region. In exploring these implications, I will then propose a hypothesis of the hippocampus as a bilateral structure. This discrete‐continuous hypothesis proposes that the left and right hippocampi contribute to spatial memory and navigation in a complementary manner. Specifically, the left hemisphere stores spatial information as discrete, salient locations, and the right hemisphere represents space continuously, contributing to route computation and flexible spatial navigation. Consideration of hippocampal lateralization in designing future studies may provide insight into the function of the hippocampus and resolve debates concerning its function.

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Learning-induced lateralized activation of the MAPK/ERK cascade in identified neurons of the food-aversion network in the mollusk Helix lucorum

Cited by 17 publications

References 55 publications

Histone H3 Acetylation is Asymmetrically Induced Upon Learning in Identified Neurons of the Food Aversion Network in the Mollusk Helix Lucorum

Histone H3 Acetylation is Asymmetrically Induced Upon Learning in Identified Neurons of the Food Aversion Network in the Mollusk Helix Lucorum

Failure of Long-Term Memory Formation in Juvenile Snails Is Determined by Acetylation Status of Histone H3 and Can Be Improved by NaB Treatment

The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization

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