Departments of Neurobiology and Anatomy and.
Bioengineering, University of Utah, Salt Lake City, Utah 84112.
J Neurosci. 2018 Feb 28;38(9):2189-2206. doi: 10.1523/JNEUROSCI.0714-17.2018. Epub 2018 Jan 26.
In mammals, olfactory sensation depends on inhalation, which controls activation of sensory neurons and temporal patterning of central activity. Odor representations by mitral and tufted (MT) cells, the main output from the olfactory bulb (OB), reflect sensory input as well as excitation and inhibition from OB circuits, which may change as sniff frequency increases. To test the impact of sampling frequency on MT cell odor responses, we obtained whole-cell recordings from MT cells in anesthetized male and female mice while varying inhalation frequency via tracheotomy, allowing comparison of inhalation-linked responses across cells. We characterized frequency effects on MT cell responses during inhalation of air and odorants using inhalation pulses and also "playback" of sniffing recorded from awake mice. Inhalation-linked changes in membrane potential were well predicted across frequency from linear convolution of 1 Hz responses; and, as frequency increased, near-identical temporal responses could emerge from depolarizing, hyperpolarizing, or multiphasic MT responses. However, net excitation was not well predicted from 1 Hz responses and varied substantially across MT cells, with some cells increasing and others decreasing in spike rate. As a result, sustained odorant sampling at higher frequencies led to increasing decorrelation of the MT cell population response pattern over time. Bulk activation of sensory inputs by optogenetic stimulation affected MT cells more uniformly across frequency, suggesting that frequency-dependent decorrelation emerges from odor-specific patterns of activity in the OB network. These results suggest that sampling behavior alone can reformat early sensory representations, possibly to optimize sensory perception during repeated sampling. Olfactory sensation in mammals depends on inhalation, which increases in frequency during active sampling of olfactory stimuli. We asked how inhalation frequency can shape the neural coding of odor information by recording from projection neurons of the olfactory bulb while artificially varying odor sampling frequency in the anesthetized mouse. We found that sampling an odor at higher frequencies led to diverse changes in net responsiveness, as measured by action potential output, that were not predicted from low-frequency responses. These changes led to a reorganization of the pattern of neural activity evoked by a given odorant that occurred preferentially during sustained, high-frequency inhalation. These results point to a novel mechanism for modulating early sensory representations solely as a function of sampling behavior.
在哺乳动物中，嗅觉感知依赖于吸入，吸入控制着感觉神经元的激活和中枢活动的时间模式。嗅球（OB）的主要输出细胞——僧帽细胞和丛状细胞（MT）对气味的表示既反映了感觉输入，也反映了 OB 回路的兴奋和抑制，而这些兴奋和抑制可能随着嗅探频率的增加而改变。为了测试采样频率对 MT 细胞气味反应的影响，我们通过气管切开术改变麻醉雄性和雌性小鼠的吸入频率，从而从细胞间比较吸入相关反应，从麻醉的雄性和雌性小鼠中获得 MT 细胞的全细胞膜片钳记录。我们使用吸入脉冲和从清醒小鼠记录的嗅探“回放”来描述 MT 细胞在吸入空气和气味剂时的频率效应。从 1 Hz 反应的线性卷积可以很好地预测跨频率的膜电位变化；并且，随着频率的增加，从去极化、超极化或多相 MT 反应中可以产生几乎相同的时间响应。然而，净兴奋不能从 1 Hz 反应中很好地预测，并且在 MT 细胞之间变化很大，有些细胞的尖峰率增加，而有些细胞的尖峰率减少。因此，在较高频率下持续采样气味会导致 MT 细胞群体反应模式随时间的相关性逐渐降低。光遗传刺激对感觉输入的整体激活在跨频率上对 MT 细胞的影响更加均匀，这表明频率相关的去相关是由 OB 网络中特定于气味的活动模式产生的。这些结果表明，采样行为本身可以重新格式化早期的感觉表示，可能是为了在重复采样期间优化感觉感知。哺乳动物的嗅觉感知依赖于吸入，在主动嗅探气味刺激时，吸入频率会增加。我们在麻醉小鼠中记录嗅球投射神经元，同时人为改变气味采样频率，以了解吸入频率如何影响气味信息的神经编码。我们发现，以较高的频率采样气味会导致动作电位输出测量的净反应性发生多样化变化，而这些变化不能从低频反应中预测。这些变化导致给定气味剂诱发的神经活动模式的重新组织，这种组织在持续的、高频的吸入过程中优先发生。这些结果指出了一种新的机制，仅通过采样行为就可以调节早期感觉表示。
