Short-term plasticity at inhibitory synapses in rat striatum and its effects on striatal output.
Two forms of short-term plasticity at inhibitory synapses were investigated in adult rat striatal brain slices using intracellular recordings. Intrastriatal stimulation in the presence of the ionotropic glutamate receptor antagonists 6-cyano-7-nitroquinoxaline-2,3-dione (20 microM) and D,L-2-amino-5-phosphonovaleric acid (50 microM) produced an inhibitory postsynaptic potential (IPSP) that reversed polarity at -76 +/- 1 (SE) mV and was sensitive to bicuculline (30 microM). The IPSP rectified at hyperpolarized membrane potentials due in part to activation of K(+) channels. The IPSP exhibited two forms of short-term plasticity, paired-pulse depression (PPD) and synaptic augmentation. PPD lasted for several seconds and was greatest at interstimulus intervals (ISIs) of several hundred milliseconds, reducing the IPSP to 80 +/- 2% of its control amplitude at an ISI of 200 ms. Augmentation of the IPSP, elicited by a conditioning train of 15 stimuli applied at 20 Hz, was 119 +/- 1% of control when sampled 2 s after the conditioning train. Augmentation decayed with a time constant of 10 s. We tested if PPD and augmentation modify the ability of the IPSP to prevent the generation of action potentials. A train of action potentials triggered by a depolarizing current injection of constant amplitude could be interrupted by stimulation of an IPSP. If this IPSP was the second in a pair of IPSPs, it was less effective in blocking spikes due to PPD. By contrast, augmented IPSPs were more effective in blocking spikes. The same results were achieved when action potentials were triggered by a depolarizing current injection of varying amplitude, a manipulation that produces nearly identical spike times from trial to trial and approximates the in vivo behavior of these neurons. These results demonstrate that short-term plasticity of inhibition can modify the output of the striatum and thus may be an important component of information processing during behaviors that involve the striatum.
Fitzpatrick
J S
JS
Leonard Davis School of Gerontology and Program in Neuroscience, University of Southern California, Los Angeles, California 90089-0191, USA.
Akopian
G
G
Walsh
J P
JP
D015763:2-Amino-5-phosphonovalerate / Q000494:pharmacology; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000200:Action Potentials / Q000187:drug effects; D000818:Animals; D001285:Atropine / Q000494:pharmacology; D001552:Benzazepines / Q000494:pharmacology; D001640:Bicuculline / Q000494:pharmacology; D002413:Cations, Divalent / Q000494:pharmacology; D003342:Corpus Striatum / Q000502:physiology*; D018492:Dopamine Antagonists / Q000494:pharmacology; D004558:Electric Stimulation; D005071:Evoked Potentials / Q000187:drug effects; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D015640:Ion Channel Gating / Q000187:drug effects; D017136:Ion Transport / Q000187:drug effects; D008845:Microinjections; D018727:Muscarinic Antagonists / Q000494:pharmacology; D009419:Nerve Tissue Proteins / Q000187:drug effects / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000187:drug effects / Q000502:physiology; D009943:Organophosphorus Compounds / Q000494:pharmacology; D018408:Patch-Clamp Techniques; D011188:Potassium / Q000378:metabolism; D015221:Potassium Channels / Q000187:drug effects / Q000502:physiology; D051381:Rats; D011916:Rats, Inbred F344; D011954:Receptors, Dopamine / Q000187:drug effects / Q000502:physiology; D011963:Receptors, GABA-A / Q000187:drug effects / Q000502:physiology; D018080:Receptors, GABA-B / Q000187:drug effects / Q000502:physiology; D011976:Receptors, Muscarinic / Q000187:drug effects / Q000502:physiology; D013469:Sulpiride / Q000494:pharmacology; D013569:Synapses / Q000187:drug effects / Q000502:physiology*
D001552:Benzazepines; D002413:Cations, Divalent; D018492:Dopamine Antagonists; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D018727:Muscarinic Antagonists; D009419:Nerve Tissue Proteins; D009943:Organophosphorus Compounds; D015221:Potassium Channels; D011954:Receptors, Dopamine; D011963:Receptors, GABA-A; D018080:Receptors, GABA-B; D011976:Receptors, Muscarinic; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D015763:2-Amino-5-phosphonovalerate; D001285:Atropine; D013469:Sulpiride; C066430:CGP 35348; D011188:Potassium; D001640:Bicuculline