Enhanced high‐frequency membrane potential fluctuations control spike output in striatal fast‐spiking interneurones in vivo

Non‐technical summary  Rhythmic activity patterns are a common theme throughout neuroscience. However, it is still poorly understood how network functions are modulated by fast oscillatory inputs from distant brain regions. In this respect, the striatum is particularly interesting as almost all neur...

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Bibliographic Details
Published in:The Journal of physiology 2011-09, Vol.589 (17), p.4365-4381
Main Authors: Schulz, Jan M., Pitcher, Toni L., Savanthrapadian, Shakuntala, Wickens, Jeffery R., Oswald, Manfred J., Reynolds, John N. J.
Format: Article
Language:English
Subjects:
Action Potentials
Animals
Corpus Striatum
Interneurons
Membrane Potentials
Neostriatum
Neurons
Neuroscience: Behavioural/Systems/Cognitive
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Summary:Non‐technical summary  Rhythmic activity patterns are a common theme throughout neuroscience. However, it is still poorly understood how network functions are modulated by fast oscillatory inputs from distant brain regions. In this respect, the striatum is particularly interesting as almost all neuronal activity is driven by long‐range inputs. We find that the three main classes of neurones in the striatum show very distinct oscillatory activity patterns in specific frequency ranges. In particular, we show that fast‐spiking interneurones are highly sensitive to fast fluctuating synaptic inputs in the intact brain. This sensitivity was probably due to a combination of faster dynamics of synaptic inputs and intrinsic amplification of high‐frequency signals. In contrast, projection neurones and other interneurones lacking these mechanisms were insensitive to fast oscillatory input patterns. These results suggest that transmission of fast cortical oscillatory inputs modulates information processing in the striatum via engagement of fast‐spiking interneurones.   Fast‐spiking interneurones (FSIs) constitute a prominent part of the inhibitory microcircuitry of the striatum; however, little is known about their recruitment by synaptic inputs in vivo. Here, we report that, in contrast to cholinergic interneurones (CINs), FSIs (n= 9) recorded in urethane‐anaesthetized rats exhibit Down‐to‐Up state transitions very similar to spiny projection neurones (SPNs). Compared to SPNs, the FSI Up state membrane potential was noisier and power spectra exhibited significantly larger power at frequencies in the gamma range (55–95 Hz). The membrane potential exhibited short and steep trajectories preceding spontaneous spike discharge, suggesting that fast input components controlled spike output in FSIs. Spontaneous spike data contained a high proportion (43.6 ± 32.8%) of small inter‐spike intervals (ISIs) of
ISSN:0022-3751
1469-7793
DOI:10.1113/jphysiol.2011.212944