Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex In vitro

doi:10.1016/0306-4522(95)00436-M

Neuroscience

Volume 70, Issue 1, January 1996, Pages 1-5

https://doi.org/10.1016/0306-4522(95)00436-M Get rights and content

Abstract

Learning deficits resulting from dopamine depletion suggest that striatal dopamine release is crucial for reinforcement. Recently described firing patterns of dopamine neurons in behaving monkeys show that transient increases in dopamine release are brought about by reinforcement. We describe an enduring change in the strength of synaptic transmission following pulsatile application of dopamine intended to mimic the transient increases associated with reinforcement. Intracellular records were made from neurons in slices of the rat corticostriatal system. Neurons having the properties of the medium-sized spiny neurons responded to cortical stimulation with depolarizing potentials (peak amplitude 12.0 ± 1.3 mV; latency 9.2 ± 0.1 ms; mean ± S.D., n = 19), which had the properties of monosynaptic excitatory postsynaptic potentials. After trains of stimuli to the cortex had been applied in conjunction with intracellular depolarizing current, the size of these excitatory postsynaptic potentials was reduced (−27% at 20 min). Application of dopamine (∼ 30 μM) in a solution containing KCl concomitant with depolarization and presynaptic activation increased the subsequent excitatory postsynaptic potentials (+ 21% at 20 min) without significant lasting change in the membrane properties of the postsynaptic cell. This suggests that dopamine has en enduring, activity-dependent action on the efficacy of corticostriatal transmission, which may be a cellular basis for the learning-related effects of the nigrostriatal system.

Reference (16)

CalabresiP. et al.
Coactivation of D₁ and D₂ dopamine receptors is required for long-term synaptic depression in the striatum
Neurosci. Lett.
(1992)
KawagoeK.T. et al.
Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum
Neuroscience
(1992)
WalshJ.P.
Depression of excitatory synaptic input in rat striatal neurons
Brain Res.
(1993)
WhishawI.Q. et al.
Dopamine depletion, stimulation or blockade in the rat disrupts spatial navigation and locomotion dependent upon beacon or distal cues
Behav. Brain Res.
(1985)
ArbuthnottG.W. et al.
The rat cortico-striatal pathway in vitro
J. Physiol. Lond.
(1985)
CalabresiP. et al.
Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels
Eur. J. Neurosci.
(1992)
CalabresiP. et al.
Transmitter release associated with long-term synaptic depression in rat corticostriatal slices
Eur. J. Neurosci.
(1995)
JiangZ.G. et al.
Membrane properties and synaptic responses of rat striatal neurons in vitro
J. Physiol.
(1991)

There are more references available in the full text version of this article.

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Abstract

Reference (16)

Coactivation of D₁ and D₂ dopamine receptors is required for long-term synaptic depression in the striatum

Neurosci. Lett.

Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum

Neuroscience

Depression of excitatory synaptic input in rat striatal neurons

Brain Res.

Dopamine depletion, stimulation or blockade in the rat disrupts spatial navigation and locomotion dependent upon beacon or distal cues

Behav. Brain Res.

The rat cortico-striatal pathway in vitro

J. Physiol. Lond.

Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels

Eur. J. Neurosci.

Transmitter release associated with long-term synaptic depression in rat corticostriatal slices

Eur. J. Neurosci.

Membrane properties and synaptic responses of rat striatal neurons in vitro

J. Physiol.

Cited by (241)

Spatiotemporal motor learning with reward-modulated Hebbian plasticity in modular reservoir computing

Synaptic plasticity during brain development: Implications for therapeutic reorganization of neural circuits

50 Years Since the Marr, Ito, and Albus Models of the Cerebellum

Contributions of the basal ganglia to action sequence learning and performance

The Meaning of Behavior: Discriminating Reflex and Volition in the Brain

Immediate and delayed auditory feedback in declarative learning: An examination of the feedback related event related potentials