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Microglial activation enhances associative taste memory through purinergic modulation of glutamatergic

Jean-Christophe Delpech¹, Nicolas Saucisse¹, Shauna L Parkes²

¹INRA, Nutrition et Neurobiologie intégrée, Unité Mixte de Recherche 1286, Bordeaux, France, University of Bordeaux, Nutrition et Neurobiologie intégrée, Unité Mixte de Recherche 1286, Bordeaux, France.

The Journal of Neuroscience : the Official Journal of the Society for Neuroscience

|February 21, 2015

Abstract:

The cerebral innate immune system is able to modulate brain functioning and cognitive processes. During activation of the cerebral innate immune system, inflammatory factors produced by microglia, such as cytokines and adenosine triphosphate (ATP), have been directly linked to modulation of glutamatergic system on one hand and learning and memory functions on the other hand. However, the cellular mechanisms by which microglial activation modulates cognitive processes are still unclear. Here, we used taste memory tasks, highly dependent on glutamatergic transmission in the insular cortex, to investigate the behavioral and cellular impacts of an inflammation restricted to this cortical area in rats. We first show that intrainsular infusion of the endotoxin lipopolysaccharide induces a local inflammation and increases glutamatergic AMPA, but not NMDA, receptor expression at the synaptic level. This cortical inflammation also enhances associative, but not incidental, taste memory through increase of glutamatergic AMPA receptor trafficking. Moreover, we demonstrate that ATP, but not proinflammatory cytokines, is responsible for inflammation-induced enhancement of both associative taste memory and AMPA receptor expression in insular cortex. In conclusion, we propose that inflammation restricted to the insular cortex enhances associative taste memory through a purinergic-dependent increase of glutamatergic AMPA receptor expression at the synapse.

Insights

Brain inflammation enhances associative taste memory by increasing AMPA receptors in the insular cortex. This effect is mediated by adenosine triphosphate (ATP), not cytokines, highlighting purinergic signaling in memory modulation.

Area of Science:

Neuroscience
Immunology
Cognitive Science

Background:

The brain's innate immune system, involving microglia, influences cognitive functions.
Microglial activation releases inflammatory factors like cytokines and adenosine triphosphate (ATP), impacting the glutamatergic system and memory.
The precise cellular mechanisms linking microglial activation to cognitive modulation remain elusive.

Purpose of the Study:

To investigate the behavioral and cellular effects of localized inflammation in the rat insular cortex on taste memory.
To elucidate the role of specific inflammatory mediators, such as ATP and cytokines, in modulating memory and synaptic plasticity.

Main Methods:

Induction of localized inflammation in the rat insular cortex using lipopolysaccharide.
Assessment of taste memory using associative and incidental tasks.
Analysis of glutamatergic AMPA and NMDA receptor expression and trafficking at the synaptic level.
Investigation of the role of ATP and proinflammatory cytokines in mediating observed effects.

Main Results:

Intrainsular lipopolysaccharide administration induced local inflammation and increased synaptic AMPA receptor expression, but not NMDA receptors.
Cortical inflammation enhanced associative taste memory, correlating with increased AMPA receptor trafficking.
Adenosine triphosphate (ATP), but not proinflammatory cytokines, was identified as the mediator responsible for enhanced associative memory and AMPA receptor expression.

Conclusions:

Localized inflammation in the insular cortex enhances associative taste memory.
This enhancement is mediated by a purinergic-dependent increase in glutamatergic AMPA receptor expression at the synapse.
The findings suggest a specific role for ATP in linking inflammation to synaptic plasticity and memory formation.

Read full analysis

Keywords:

AMPA ATP cytokines lipopolysaccharide neuroinflammation

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