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.
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Self-organized critical states (SOCs) and stochastic oscillations (SOs) are simultaneously observed in neural systems, which appears to be theoretically contradictory since SOCs are characterized by scale-free avalanche sizes but oscillations indicate typical scales. Here, we show that SOs can emerge in SOCs of small size systems due to temporal correlation between large avalanches at the finite-size cutoff, resulting from the accumulation-release process in SOCs. In contrast, the critical branching process without accumulation-release dynamics cannot exhibit oscillations. The reconciliation of SOCs and SOs is demonstrated both in the sandpile model and robustly in biologically plausible neuronal networks. The oscillations can be suppressed if external inputs eliminate the prominent slow accumulation process, providing a potential explanation of the widely studied Berger effect or event-related desynchronization in neural response. The features of neural oscillations and suppression are confirmed during task processing in monkey eye-movement experiments. Our results suggest that finite-size, columnar neural circuits may play an important role in generating neural oscillations around the critical states, potentially enabling functional advantages of both SOCs and oscillations for sensitive response to transient stimuli. DOI: 10.1103/PhysRevLett.116.018101 Self-organized criticality [1] is a key concept for describing the emergence of complexity in many natural systems [2]. The fingerprint of self-organized critical states (SOCs), the power-law distribution of avalanche sizes, means that the activity has no characteristic scale in the thermodynamic limit. As excellent functional complex systems in nature, neural systems in the brain have been supposed to operate at SOCs. Indeed, SOCs of neuronal firing activity have been observed in experiments with electrode arrays [2-4] and have been studied intensively in computational models [2,5,6]. It has been shown that critical states have functional advantages for both the sensory system [7] and memory [8], and they play an important role in the development of neural systems [9].On the other hand, stochastic oscillation (SO) in brain activity has been observed for more than 80 years [10]. Oscillations characterized by repetition of activities with typical scales are believed to be essential to brain functions, especially to provide timing, predictability, coherence, and integration in neural information processing [11]. Several different oscillation bands exist and appear in different states of the brain [10]. The synchronization between inhibitory neurons has been found to be crucial for gamma oscillations (30-70 Hz) [12]. Neural field models [13] indicated that resonance between thalamus and cortex can generate alpha oscillations (8-13 Hz). Despite many modeling studies, a commonly accepted mechanism of alpha rhythm is still lacking [14]. This slow oscillation is particularly obvious during the resting states without systematic external stimuli (i.e., eyes closed). I...
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