Abstract
Cortical fast-spiking (FS) neurons generate high-frequency action potentials (APs) without apparent frequency accommodation, thus providing fast and precise inhibition. However, the maximal firing frequency that they can reach, particularly in primate neocortex, remains unclear. Here, by recording in human, monkey, and mouse neocortical slices, we revealed that FS neurons in human association cortices (mostly temporal) could generate APs at a maximal mean frequency (Fmean) of 338 Hz and a maximal instantaneous frequency (Finst) of 453 Hz, and they increase with age. The maximal firing frequency of FS neurons in the association cortices (frontal and temporal) of monkey was even higher (Fmean 450 Hz, Finst 611 Hz), whereas in the association cortex (entorhinal) of mouse it was much lower (Fmean 215 Hz, Finst 342 Hz). Moreover, FS neurons in mouse primary visual cortex (V1) could fire at higher frequencies (Fmean 415 Hz, Finst 582 Hz) than those in association cortex. We further validated our in vitro data by examining spikes of putative FS neurons in behaving monkey and mouse. Together, our results demonstrate that the maximal firing frequency of FS neurons varies between species and cortical areas.
Highlights
Neocortical fast-spiking (FS) neurons have been well-identified on the basis of their highly uniform electrophysiological characteristics, including the narrowest action potential (AP) among cortical neurons, fast membrane passive kinetics and their ability to generate high-frequency action potentials (APs) trains with very little frequency accommodation (McCormick et al, 1985; Connors and Gutnick, 1990), known as the non-accommodating neurons
FS neurons were identified by their narrow APs and little steady-state firingfrequency accommodation
The second subtype fired AP burst at the beginning, termed the bursting FS (b-FS) neurons
Summary
Neocortical fast-spiking (FS) neurons have been well-identified on the basis of their highly uniform electrophysiological characteristics, including the narrowest action potential (AP) among cortical neurons, fast membrane passive kinetics and their ability to generate high-frequency AP trains with very little frequency accommodation (McCormick et al, 1985; Connors and Gutnick, 1990), known as the non-accommodating neurons. Some other passive and active properties of neuronal membrane contribute to the fast generation and propagation of electric signals in FS neurons (Hu and Jonas, 2014), including. The feedforward inhibition mediated by FS neurons is responsible for the temporal precision of postsynaptic APs by limiting the time window of EPSP integration (Pouille and Scanziani, 2001), and expanding the dynamic range of neural circuits by gain control (Pouille et al, 2009; Atallah et al, 2012; Wilson et al, 2012). FS neurons control the spatial and temporal precision of sensory information processing, by providing cortical feedback and lateral inhibition (Cardin et al, 2009; Couey et al, 2013)
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