Greater excitability and firing irregularity of tufted cells underlies distinct afferent-evoked activity of olfactory bulb mitral and tufted cells

Greater excitability and firing irregularity of tufted cells underlies distinct afferent-evoked activity of olfactory bulb mitral and tufted cells
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DOI:
10.1113/jphysiol.2013.269886
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发表时间:
2014-05-15
影响因子:
5.5
通讯作者:
Urban, Nathaniel N.
Urban, Nathaniel N.
中科院分区:
医学1区
文献类型:
--
作者:
Burton, Shawn D.;Urban, Nathaniel N.

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要点哺乳动物主嗅球中的两类主要神经元,即二尖瓣细胞和簇状细胞,对传入诱发的输入以不同的放电潜伏期和速率做出反应;这些活动差异是如何产生的尚不完全清楚。簇状细胞比二尖瓣细胞接收更强的传入诱发兴奋,但仅这种差异不足以解释簇状细胞与二尖瓣细胞相比更强的传入诱发放电。二尖瓣细胞和簇状细胞表现出显着的内在功能差异;与二尖瓣细胞相比,簇状细胞以更短的持续时间和更快的后超极化激发动作电位,并表现出两倍的放电速率-电流曲线增益和峰值速率。簇状细胞表现出多种放电模式,包括强直放电和不规则口吃,并且平均放电比二尖瓣细胞更加不规则。总的来说,簇状细胞中更强的传入兴奋、更大的内在兴奋性和更不规则的放电结合起来,驱动二尖瓣和簇状细胞对感觉输入的不同反应。二尖瓣细胞和簇状细胞是哺乳动物主嗅球中的两类主要神经元,表现出形态差异,但仍然被广泛认为在功能上是等效的。然而,最近几项研究的结果表明,这两种细胞类别可能以其不同的传入诱发活动模式编码互补的嗅觉信息。为了了解这些活性差异是如何产生的,我们对二尖瓣细胞和簇状细胞之间的突触和内在特性进行了首次系统比较。与之前的研究一致,我们发现簇状细胞响应生理传入刺激的概率和速率比二尖瓣细胞更高,并且延迟更短。簇状细胞的这种更强的反应可能部分归因于突触差异,因为簇状细胞比二尖瓣细胞接受更强的传入诱发兴奋。然而,内在兴奋性的差异也导致了二尖瓣细胞和簇状细胞活性之间的差异。与二尖瓣细胞相比,簇状细胞表现出两倍的兴奋性和峰值瞬时放电率。这些兴奋性差异可能源于电压门控钾电流的差异表达,因为簇状细胞比二尖瓣细胞表现出更快的动作电位复极化和后超极化。令人惊讶的是,二尖瓣细胞和簇状细胞也表现出放电模式差异。虽然这两类细胞都表现出动作电位簇的规则放电和不规则口吃,但簇状细胞比二尖瓣细胞表现出更大的口吃倾向。总的来说,簇状细胞中更强的传入诱发兴奋、更大的内在兴奋性和更不规则的放电可以结合起来驱动二尖瓣和簇状细胞对传入诱发输入的不同反应。
Key pointsThe two classes of principal neurons in the mammalian main olfactory bulb, mitral and tufted cells, respond with different firing latencies and rates to afferent-evoked input; how these differences in activity arise is incompletely understood. Tufted cells receive stronger afferent-evoked excitation than mitral cells, but this difference alone is insufficient to account for the greater afferent-evoked firing in tufted versus mitral cells. Mitral and tufted cells exhibit significant intrinsic functional differences; compared to mitral cells, tufted cells fire action potentials with shorter durations and faster afterhyperpolarizations and exhibit twofold greater firing rate-current curve gains and peak rates. Tufted cells exhibit diverse firing modes, including tonic firing and irregular stuttering, and on average fire more irregularly than mitral cells. Collectively, stronger afferent excitation, greater intrinsic excitability and more irregular firing in tufted cells combine to drive distinct responses of mitral and tufted cells to sensory input. Mitral and tufted cells, the two classes of principal neurons in the mammalian main olfactory bulb, exhibit morphological differences but remain widely viewed as functionally equivalent. Results from several recent studies, however, suggest that these two cell classes may encode complementary olfactory information in their distinct patterns of afferent-evoked activity. To understand how these differences in activity arise, we have performed the first systematic comparison of synaptic and intrinsic properties between mitral and tufted cells. Consistent with previous studies, we found that tufted cells fire with higher probability and rates and shorter latencies than mitral cells in response to physiological afferent stimulation. This stronger response of tufted cells could be partially attributed to synaptic differences, as tufted cells received stronger afferent-evoked excitation than mitral cells. However, differences in intrinsic excitability also contributed to the differences between mitral and tufted cell activity. Compared to mitral cells, tufted cells exhibited twofold greater excitability and peak instantaneous firing rates. These differences in excitability probably arise from differential expression of voltage-gated potassium currents, as tufted cells exhibited faster action potential repolarization and afterhyperpolarizations than mitral cells. Surprisingly, mitral and tufted cells also showed firing mode differences. While both cell classes exhibited regular firing and irregular stuttering of action potential clusters, tufted cells demonstrated a greater propensity to stutter than mitral cells. Collectively, stronger afferent-evoked excitation, greater intrinsic excitability and more irregular firing in tufted cells can combine to drive distinct responses of mitral and tufted cells to afferent-evoked input.