Dataset Information

Uncoordinated firing rate changes of striatal fast-spiking interneurons during behavioral task performance.

ABSTRACT: Basal ganglia circuits make key contributions to decision making. Distributed, synchronous feedforward inhibition of striatal medium spiny neurons by fast-spiking GABAergic interneurons (FSIs) has been argued to be important for the suppression of unwanted actions, and a deficit in FSIs has been found in human patients with Tourette syndrome. However, no studies have yet examined how striatal FSIs change their activity during behavioral tasks. Here I describe 36 presumed striatal FSIs recorded in rats during well practiced performance of a radial maze win-stay task. Although most FSIs showed robust task-related activity, the temporal patterns of firing rate change were highly idiosyncratic. In contrast to other classes of striatal neurons, FSIs showed little or no coordinated population response to major task events such as instruction cues or rewards. Even when multiple FSIs were recorded simultaneously from the same local region of striatum, firing rate changes were dissimilar, and no clear evidence for synchronous firing was found using cross-correlograms (18 FSI pairs examined). These results suggest that FSIs play a more complex role in the information processing achieved by striatal microcircuits than supposed by current theoretical models.

SUBMITTER: Berke JD

PROVIDER: S-EPMC2613805 | biostudies-literature | 2008 Oct

REPOSITORIES: biostudies-literature

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Uncoordinated firing rate changes of striatal fast-spiking interneurons during behavioral task performance.

Berke Joshua D JD

The Journal of neuroscience : the official journal of the Society for Neuroscience 20081001 40

Basal ganglia circuits make key contributions to decision making. Distributed, synchronous feedforward inhibition of striatal medium spiny neurons by fast-spiking GABAergic interneurons (FSIs) has been argued to be important for the suppression of unwanted actions, and a deficit in FSIs has been found in human patients with Tourette syndrome. However, no studies have yet examined how striatal FSIs change their activity during behavioral tasks. Here I describe 36 presumed striatal FSIs recorded i ...[more]

PMID: 18829965

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Project description:Striatal fast-spiking interneurons (FSIs) fire in variable-length runs of action potentials at 20-200 spikes/s separated by pauses. In vivo, or with fluctuating applied current, both runs and pauses become briefer and more variable. During runs, spikes are entrained specifically to gamma-frequency components of the input fluctuations. We stimulated parvalbumin-expressing striatal FSIs in mouse brain slices with broadband noise currents added to direct current steps and measured spike entrainment across all frequencies. As the constant current level was increased, FSIs produced longer runs and showed sharper frequency tuning, with best entrainment at the stimulus frequency matching their intrarun firing rate. We separated the contributions of previous spikes from that of the fluctuating stimulus, revealing a strong contribution of previous action potentials to gamma-frequency entrainment. In contrast, after subtraction of the effect inherited from the previous spike, the remaining stimulus contribution to spike generation was less sharply tuned, showing a larger contribution of lower frequencies. The frequency specificity of entrainment within a run was reproduced with a phase resetting model based on experimentally measured phase resetting curves of the same FSIs. In the model, broadly tuned phase entrainment for the first spike in a run evolved into sharply tuned gamma entrainment over the next few spikes. The data and modeling results indicate that for FSIs firing in brief runs and pauses firing within runs is entrained by gamma-frequency components of the input, whereas the onset timing of runs may be sensitive to a wider range of stimulus frequency components.NEW & NOTEWORTHY Specific types of neurons entrain their spikes to particular oscillation frequencies in their synaptic input. This entrainment is commonly understood in terms of the subthreshold voltage response, but how this translates to spiking is not clear. We show that in striatal fast-spiking interneurons, entrainment to gamma-frequency input depends on rhythmic spike runs and is explained by the phase resetting curve, whereas run initiation can be triggered by a broad range of input frequencies.

Dataset Information

Uncoordinated firing rate changes of striatal fast-spiking interneurons during behavioral task performance.

Publications

Uncoordinated firing rate changes of striatal fast-spiking interneurons during behavioral task performance.

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