TY - JOUR
T1 - Facilitation of corticostriatal plasticity by the amygdala requires Ca 2+-induced Ca2+ release in the ventral striatum
AU - Popescu, Andrei T.
AU - Saghyan, Aleksandr A.
AU - Nagy, Frank Z.
AU - Paré, Denis
PY - 2010/9
Y1 - 2010/9
N2 - Motor learning and habit formation are thought to depend on corticostriatal synaptic plasticity. Moreover, basolateral amygdala (BLA) activity facilitates consolidation of striatal-dependent memories. Accordingly, BLA stimulation in vitro facilitates long-term potentiation (LTP) induction at corticostriatal synapses onto medium spiny neurons (MSNs). Although these effects were found to depend on N-methyl-D-aspartate (NMDA) receptor activation at BLA synapses and consequent Ca2+ influx, it is unclear how this event can facilitate LTP at cortical synapses, even when the two inputs are not coactivated. Here, we aimed to shed light on this question, using whole cell recordings of MSNs in vitro. We first tested whether BLA inputs end at more proximal dendritic sites than cortical inputs. In this scenario, BLA synapses would experience stronger spike-related depolarizations and be in a strategic position to control the spread of second messengers. However, comparison of compound excitatory postsynaptic potentials and single-axon excitatory postsynaptic currents revealed that BLA and cortical synapses are intermingled. Next, we examined the sensitivity of cortical and BLA NMDA responses to ifenprodil because NR2A-containing NMDA receptors have faster kinetics than those containing NR2B subunits. However, the two inputs did not differ in this respect. Last, reasoning that propagating waves of Ca2+-induced Ca2+ release (CICR) could bridge temporal gaps between the two inputs, we tested the effects of CICR inhibitors on the BLA facilitation of corticostriatal LTP induction. Pharmacological interference with CICR blocked corticostriatal LTP induction. Thus our results are consistent with the notion that NMDA-dependent Ca2+ influx at BLA synapses initiates propagating waves of CICR, thereby biasing active corticostriatal inputs toward synaptic potentiation.
AB - Motor learning and habit formation are thought to depend on corticostriatal synaptic plasticity. Moreover, basolateral amygdala (BLA) activity facilitates consolidation of striatal-dependent memories. Accordingly, BLA stimulation in vitro facilitates long-term potentiation (LTP) induction at corticostriatal synapses onto medium spiny neurons (MSNs). Although these effects were found to depend on N-methyl-D-aspartate (NMDA) receptor activation at BLA synapses and consequent Ca2+ influx, it is unclear how this event can facilitate LTP at cortical synapses, even when the two inputs are not coactivated. Here, we aimed to shed light on this question, using whole cell recordings of MSNs in vitro. We first tested whether BLA inputs end at more proximal dendritic sites than cortical inputs. In this scenario, BLA synapses would experience stronger spike-related depolarizations and be in a strategic position to control the spread of second messengers. However, comparison of compound excitatory postsynaptic potentials and single-axon excitatory postsynaptic currents revealed that BLA and cortical synapses are intermingled. Next, we examined the sensitivity of cortical and BLA NMDA responses to ifenprodil because NR2A-containing NMDA receptors have faster kinetics than those containing NR2B subunits. However, the two inputs did not differ in this respect. Last, reasoning that propagating waves of Ca2+-induced Ca2+ release (CICR) could bridge temporal gaps between the two inputs, we tested the effects of CICR inhibitors on the BLA facilitation of corticostriatal LTP induction. Pharmacological interference with CICR blocked corticostriatal LTP induction. Thus our results are consistent with the notion that NMDA-dependent Ca2+ influx at BLA synapses initiates propagating waves of CICR, thereby biasing active corticostriatal inputs toward synaptic potentiation.
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U2 - 10.1152/jn.00233.2010
DO - 10.1152/jn.00233.2010
M3 - Article
C2 - 20554836
AN - SCOPUS:77957204635
SN - 0022-3077
VL - 104
SP - 1673
EP - 1680
JO - Journal of neurophysiology
JF - Journal of neurophysiology
IS - 3
ER -