Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses.

TY - JOUR

T1 - Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses.

AU - Holbro, Niklaus

AU - Grunditz, Asa

AU - Oertner, Thomas G.

PY - 2009

Y1 - 2009

N2 - Synaptic plasticity is considered essential for learning and storage of new memories. Whether all synapses on a given neuron have the same ability to express long-term plasticity is not well understood. Synaptic microanatomy could affect the function of local signaling cascades and thus differentially regulate the potential for plasticity at individual synapses. Here, we investigate how the presence of endoplasmic reticulum (ER) in dendritic spines of CA1 pyramidal neurons affects postsynaptic signaling. We show that the ER is targeted selectively to large spines containing strong synapses. In ER-containing spines, we frequently observed synaptically triggered calcium release events of very large amplitudes. Low-frequency stimulation of these spines induced a permanent depression of synaptic potency that was independent of NMDA receptor activation and specific to the stimulated synapses. In contrast, no functional changes were induced in the majority of spines lacking ER. Both calcium release events and long-term depression depended on the activation of metabotropic glutamate receptors and inositol trisphosphate receptors. In summary, spine microanatomy is a reliable indicator for the presence of specific signaling cascades that govern plasticity on a micrometer scale.

AB - Synaptic plasticity is considered essential for learning and storage of new memories. Whether all synapses on a given neuron have the same ability to express long-term plasticity is not well understood. Synaptic microanatomy could affect the function of local signaling cascades and thus differentially regulate the potential for plasticity at individual synapses. Here, we investigate how the presence of endoplasmic reticulum (ER) in dendritic spines of CA1 pyramidal neurons affects postsynaptic signaling. We show that the ER is targeted selectively to large spines containing strong synapses. In ER-containing spines, we frequently observed synaptically triggered calcium release events of very large amplitudes. Low-frequency stimulation of these spines induced a permanent depression of synaptic potency that was independent of NMDA receptor activation and specific to the stimulated synapses. In contrast, no functional changes were induced in the majority of spines lacking ER. Both calcium release events and long-term depression depended on the activation of metabotropic glutamate receptors and inositol trisphosphate receptors. In summary, spine microanatomy is a reliable indicator for the presence of specific signaling cascades that govern plasticity on a micrometer scale.

KW - Animals

KW - Rats

KW - Rats, Wistar

KW - Calcium/metabolism

KW - Endoplasmic Reticulum/metabolism

KW - Hippocampus/cytology/metabolism

KW - Neuronal Plasticity

KW - Receptors, Metabotropic Glutamate/metabolism

KW - Receptors, N-Methyl-D-Aspartate/metabolism

KW - Signal Transduction

KW - Synapses/metabolism

KW - Tissue Culture Techniques

KW - Animals

KW - Rats

KW - Rats, Wistar

KW - Calcium/metabolism

KW - Endoplasmic Reticulum/metabolism

KW - Hippocampus/cytology/metabolism

KW - Neuronal Plasticity

KW - Receptors, Metabotropic Glutamate/metabolism

KW - Receptors, N-Methyl-D-Aspartate/metabolism

KW - Signal Transduction

KW - Synapses/metabolism

KW - Tissue Culture Techniques

M3 - SCORING: Journal article

VL - 106

SP - 15055

EP - 15060

JO - P NATL ACAD SCI USA

JF - P NATL ACAD SCI USA

SN - 0027-8424

IS - 35

M1 - 35

ER -