Fast synaptic transmission between striatal spiny projection neurons.
Striatal inhibition plays an important role in models of cortex-basal ganglia function and is altered in many basal ganglia diseases. The gamma-aminobutyric acid ergic spiny projection neuron comprises >95% of striatal neurons, but despite strong anatomical evidence, the electrophysiological properties and functions of their local axon collaterals are unknown. We simultaneously recorded from adjacent spiny projection neurons (<5-10 microm) in whole-cell patch mode and demonstrated a fast synaptic connection between 2669 pairs in cortex-striatum-substantia nigra organotypic cultures and 538 pairs in acute striatal slices. The synapse, which was blocked by gamma-aminobutyric acid type A antagonists, displayed a wide range of failure rates, was depolarizing at rest, and reversed above -60 mV. Presynaptic bursts of action potentials were highly correlated with total postsynaptic depolarization at rest. Synaptic transmission was optimized for burst discharge >14 Hz and showed considerable short-term plasticity, including paired-pulse depression at intervals <25 ms, intraburst facilitation, and interburst augmentation. This activity-dependent collateral interaction provides the basis for a new class of basal ganglia models in which striatal neurons cooperate as well as compete during processing of cortical inputs.
Czubayko
Uwe
U
Unit of Neural Network Physiology, Laboratory of Systems Neuroscience, National Institute of Mental Health, 9000 Rockville Pike, Bethesda, MD 20892, USA.
Plenz
Dietmar
D
D000200:Action Potentials / Q000187:drug effects; D000818:Animals; D001640:Bicuculline / Q000031:analogs & derivatives* / Q000494:pharmacology; D002540:Cerebral Cortex / Q000166:cytology; D003342:Corpus Striatum / Q000166:cytology*; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D008570:Memory, Short-Term / Q000502:physiology; D009474:Neurons / Q000145:classification / Q000187:drug effects / Q000502:physiology*; D009924:Organ Culture Techniques; D018408:Patch-Clamp Techniques; D010852:Picrotoxin / Q000494:pharmacology; D011810:Quinoxalines / Q000494:pharmacology; D051381:Rats; D013378:Substantia Nigra / Q000166:cytology; D013569:Synapses / Q000502:physiology; D009435:Synaptic Transmission / Q000187:drug effects; D005680:gamma-Aminobutyric Acid / Q000502:physiology
D001640:Bicuculline; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D010852:Picrotoxin; D011810:Quinoxalines; D005680:gamma-Aminobutyric Acid; C017069:bicuculline methiodide; C056723:FG 9041