Cholinergic interneurons control the excitatory input to the striatum.
How the extent and time course of presynaptic inhibition depend on the action potentials of the neuron controlling the terminals is unknown. We investigated this issue in the striatum using paired recordings from cholinergic interneurons and projection neurons. Glutamatergic EPSCs were evoked in projection neurons and cholinergic interneurons by stimulation of afferent fibers in the cortex and the striatum, respectively. A single spike in a cholinergic interneuron caused significant depression of the evoked glutamatergic EPSC in 34% of projection neurons located within 100 microm and 41% of cholinergic interneurons located within 200 microm. The time course of these effects was similar in the two cases, with EPSC inhibition peaking 20-30 ms after the spike and disappearing after 40-80 ms. Maximal depression of EPSC amplitude was up to 27% in projection neurons and to 19% in cholinergic interneurons. These effects were reversibly blocked by muscarinic receptor antagonists (atropine or methoctramine), which also significantly increased baseline EPSC (evoked without a preceding spike in the cholinergic interneuron), suggesting that some tonic cholinergic presynaptic inhibition was present. This was confirmed by the fact that lowering extracellular potassium, which silenced spontaneously active cholinergic interneurons, also increased baseline EPSC amplitude, and these effects were occluded by previous application of muscarinic receptor antagonists. Collectively, these results show that a single spike in a cholinergic interneuron exerts a fast and powerful inhibitory control over the glutamatergic input to striatal neurons.
Pakhotin
Pavel
P
Faculty of Life Sciences, University of Manchester, Manchester M60 1QD, United Kingdom.
Bracci
Enrico
E
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002799:Cholinergic Fibers / Q000502:physiology*; D003342:Corpus Striatum / Q000502:physiology*; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology*; D005260:Female; D007395:Interneurons / Q000502:physiology*; D008297:Male; D009434:Neural Pathways / Q000502:physiology; D051381:Rats; D017208:Rats, Wistar