scholarly journals Author response: Serotonin enhances excitability and gamma frequency temporal integration in mouse prefrontal fast-spiking interneurons

2017 ◽  
Author(s):  
Jegath C Athilingam ◽  
Roy Ben-Shalom ◽  
Caroline M Keeshen ◽  
Vikaas S Sohal ◽  
Kevin J Bender
eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jegath C Athilingam ◽  
Roy Ben-Shalom ◽  
Caroline M Keeshen ◽  
Vikaas S Sohal ◽  
Kevin J Bender

The medial prefrontal cortex plays a key role in higher order cognitive functions like decision making and social cognition. These complex behaviors emerge from the coordinated firing of prefrontal neurons. Fast-spiking interneurons (FSIs) control the timing of excitatory neuron firing via somatic inhibition and generate gamma (30–100 Hz) oscillations. Therefore, factors that regulate how FSIs respond to gamma-frequency input could affect both prefrontal circuit activity and behavior. Here, we show that serotonin (5HT), which is known to regulate gamma power, acts via 5HT2A receptors to suppress an inward-rectifying potassium conductance in FSIs. This leads to depolarization, increased input resistance, enhanced spiking, and slowed decay of excitatory post-synaptic potentials (EPSPs). Notably, we found that slowed EPSP decay preferentially enhanced temporal summation and firing elicited by gamma frequency inputs. These findings show how changes in passive membrane properties can affect not only neuronal excitability but also the temporal filtering of synaptic inputs.


Author(s):  
Justin K O'Hare ◽  
Haofang Li ◽  
Namsoo Kim ◽  
Erin Gaidis ◽  
Kristen Ade ◽  
...  

2019 ◽  
Vol 122 (3) ◽  
pp. 1060-1072 ◽  
Author(s):  
Matthew H. Higgs ◽  
Charles J. Wilson

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.


2011 ◽  
Vol 106 (6) ◽  
pp. 2936-2949 ◽  
Author(s):  
Giuseppe Sciamanna ◽  
Charles J. Wilson

Striatal fast-spiking (FS) cells in slices fire in the gamma frequency range and in vivo are often phase-locked to gamma oscillations in the field potential. We studied the firing patterns of these cells in slices from rats ages 16–23 days to determine the mechanism of their gamma resonance. The resonance of striatal FS cells was manifested as a minimum frequency for repetitive firing. At rheobase, cells fired a doublet of action potentials or doublets separated by pauses, with an instantaneous firing rate averaging 44 spikes/s. The minimum rate for sustained firing was also responsible for the stuttering firing pattern. Firing rate adapted during each episode of firing, and bursts were terminated when firing was reduced to the minimum sustainable rate. Resonance and stuttering continued after blockade of Kv3 current using tetraethylammonium (0.1–1 mM). Both gamma resonance and stuttering were strongly dependent on Kv1 current. Blockade of Kv1 channels with dendrotoxin-I (100 nM) completely abolished the stuttering firing pattern, greatly lowered the minimum firing rate, abolished gamma-band subthreshold oscillations, and slowed spike frequency adaptation. The loss of resonance could be accounted for by a reduction in potassium current near spike threshold and the emergence of a fixed spike threshold. Inactivation of the Kv1 channel combined with the minimum firing rate could account for the stuttering firing pattern. The resonant properties conferred by this channel were shown to be adequate to account for their phase-locking to gamma-frequency inputs as seen in vivo.


2018 ◽  
Author(s):  
Elizabeth Nicholson ◽  
Dmitry A Kuzmin ◽  
Marco Leite ◽  
Thomas E Akam ◽  
Dimitri Michael Kullmann

Author(s):  
Hugo Zeberg ◽  
Nathan W. Gouwens ◽  
Kunichika Tsumoto ◽  
Takashi Tateno ◽  
Kazuyuki Aihara ◽  
...  

1999 ◽  
Vol 82 (4) ◽  
pp. 1855-1864 ◽  
Author(s):  
Rolf H. Joho ◽  
Chi Shun Ho ◽  
Gerald A. Marks

Kv3.1 is a voltage-gated, fast activating/deactivating potassium (K+) channel with a high-threshold of activation and a large unit conductance. Kv3.1 K+ channels are expressed in fast-spiking, parvalbumin-containing interneurons in cortex, hippocampus, striatum, the thalamic reticular nucleus (TRN), and in several nuclei of the brain stem. A high density of Kv3.1 channels contributes to short-duration action potentials, fast afterhyperpolarizations, and brief refractory periods enhancing the capability in these neurons for high-frequency firing. Kv3.1 K+ channel expression in the TRN and cortex also suggests a role in thalamocortical and cortical function. Here we show that fast gamma and slow delta oscillations recorded from the somatomotor cortex are altered in the freely behaving Kv3.1 mutant mouse. Electroencephalographic (EEG) recordings from homozygous Kv3.1−/− mice show a three- to fourfold increase in both absolute and relative spectral power in the gamma frequency range (20–60 Hz). In contrast, Kv3.1-deficient mice have a 20–50% reduction of power in the slow delta range (2–3 Hz). The increase in gamma power is most prominent during waking in the 40- to 55-Hz range, whereas the decrease in delta power occurs equally across all states of arousal. Our findings suggest that Kv3.1-expressing neurons are involved in the generation and maintenance of cortical fast gamma and slow delta oscillations. Hence the Kv3.1-mutant mouse could serve as a model to study the generation and maintenance of fast gamma and slow delta rhythms and their involvement in behavior and cognition.


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