Firing Frequency Maxima of Fast-Spiking Neurons in Human, Monkey, and Mouse Neocortex

Overview

Journal Front Cell Neurosci

Specialty Cell Biology

Date 2016 Nov 3

PMID 27803650

Citations 38

Authors

Bo Wang

Wei Ke

Jing Guang

Guang Chen

Luping Yin

Suixin Deng

Quansheng He

Yaping Liu

Ting He

Rui Zheng

Yanbo Jiang

Xiaoxue Zhang

Tianfu Li

Guoming Luan

Haidong D Lu

Mingsha Zhang

Xiaohui Zhang

Yousheng Shu

Affiliations

Soon will be listed here.

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 (F) of 338 Hz and a maximal instantaneous frequency (F) 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 (F 450 Hz, F 611 Hz), whereas in the association cortex (entorhinal) of mouse it was much lower (F 215 Hz, F 342 Hz). Moreover, FS neurons in mouse primary visual cortex (V1) could fire at higher frequencies (F 415 Hz, F 582 Hz) than those in association cortex. We further validated our 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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References

Galarreta M, HESTRIN S . Spike transmission and synchrony detection in networks of GABAergic interneurons. Science. 2001; 292(5525):2295-9. DOI: 10.1126/science.1061395. View

Wang B, Yin L, Zou X, Ye M, Liu Y, He T . A Subtype of Inhibitory Interneuron with Intrinsic Persistent Activity in Human and Monkey Neocortex. Cell Rep. 2015; 10(9):1450-1458. DOI: 10.1016/j.celrep.2015.02.018. View

Niell C, Stryker M . Modulation of visual responses by behavioral state in mouse visual cortex. Neuron. 2010; 65(4):472-9. PMC: 3184003. DOI: 10.1016/j.neuron.2010.01.033. View

Goldberg E, Jeong H, Kruglikov I, Tremblay R, Lazarenko R, Rudy B . Rapid developmental maturation of neocortical FS cell intrinsic excitability. Cereb Cortex. 2010; 21(3):666-82. PMC: 3041012. DOI: 10.1093/cercor/bhq138. View

Miller M, Okaty B, Kato S, Nelson S . Activity-dependent changes in the firing properties of neocortical fast-spiking interneurons in the absence of large changes in gene expression. Dev Neurobiol. 2010; 71(1):62-70. PMC: 3059083. DOI: 10.1002/dneu.20811. View

Wang Y, Gupta A, Toledo-Rodriguez M, Wu C, Markram H . Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex. 2002; 12(4):395-410. DOI: 10.1093/cercor/12.4.395. View

Foehring R, Lorenzon N, HERRON P, Wilson C . Correlation of physiologically and morphologically identified neuronal types in human association cortex in vitro. J Neurophysiol. 1991; 66(6):1825-37. DOI: 10.1152/jn.1991.66.6.1825. View

Disterhoft J, Matthew Oh M . Learning, aging and intrinsic neuronal plasticity. Trends Neurosci. 2006; 29(10):587-99. DOI: 10.1016/j.tins.2006.08.005. View

Geiger J, Lubke J, Roth A, Frotscher M, Jonas P . Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron. 1997; 18(6):1009-23. DOI: 10.1016/s0896-6273(00)80339-6. View

10.

Gonchar Y, Wang Q, Burkhalter A . Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. 2008; 1:3. PMC: 2525923. DOI: 10.3389/neuro.05.003.2007. View

11.

Shu Y, Duque A, Yu Y, Haider B, McCormick D . Properties of action-potential initiation in neocortical pyramidal cells: evidence from whole cell axon recordings. J Neurophysiol. 2006; 97(1):746-60. DOI: 10.1152/jn.00922.2006. View

12.

McCormick D, Connors B, Lighthall J, Prince D . Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 1985; 54(4):782-806. DOI: 10.1152/jn.1985.54.4.782. View

13.

Li K, Lu Y, Xu Z, Zhang J, Zhu J, Zhang J . Neuregulin 1 regulates excitability of fast-spiking neurons through Kv1.1 and acts in epilepsy. Nat Neurosci. 2011; 15(2):267-73. DOI: 10.1038/nn.3006. View

14.

Bartos M, Vida I, Jonas P . Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 2006; 8(1):45-56. DOI: 10.1038/nrn2044. View

15.

Vacher H, Mohapatra D, Trimmer J . Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol Rev. 2008; 88(4):1407-47. PMC: 2587220. DOI: 10.1152/physrev.00002.2008. View

16.

Inoue S, Matsuzawa T . Working memory of numerals in chimpanzees. Curr Biol. 2007; 17(23):R1004-5. DOI: 10.1016/j.cub.2007.10.027. View

17.

Rudy B, McBain C . Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci. 2001; 24(9):517-26. DOI: 10.1016/s0166-2236(00)01892-0. View

18.

Yang J, Zhang J, Yu Y, Duan S, Li X . Postnatal development of 2 microcircuits involving fast-spiking interneurons in the mouse prefrontal cortex. Cereb Cortex. 2012; 24(1):98-109. DOI: 10.1093/cercor/bhs291. View

19.

Cardin J, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K . Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 2009; 459(7247):663-7. PMC: 3655711. DOI: 10.1038/nature08002. View

20.

Nunez A, Amzica F, Steriade M . Electrophysiology of cat association cortical cells in vivo: intrinsic properties and synaptic responses. J Neurophysiol. 1993; 70(1):418-30. DOI: 10.1152/jn.1993.70.1.418. View