Department of Biology, West Virginia University, Morgantown, WV 26505.
eNeuro. 2018 Oct 4;5(5). doi: 10.1523/ENEURO.0212-18.2018. eCollection 2018 Sep-Oct.
Broad neuronal classes are surprisingly heterogeneous across many parameters, and subclasses often exhibit partially overlapping traits including transmitter coexpression. However, the extent to which transmitter coexpression occurs in predictable, consistent patterns is unknown. Here, we demonstrate that pairwise coexpression of GABA and multiple neuropeptide families by olfactory local interneurons (LNs) of the moth is highly heterogeneous, with a single LN capable of expressing neuropeptides from at least four peptide families and few instances in which neuropeptides are consistently coexpressed. Using computational modeling, we demonstrate that observed coexpression patterns cannot be explained by independent probabilities of expression of each neuropeptide. Our analyses point to three organizing principles that, once taken into consideration, allow replication of overall coexpression structure: (1) peptidergic neurons are highly likely to coexpress GABA; (2) expression probability of allatotropin depends on myoinhibitory peptide expression; and (3) the all-or-none coexpression patterns of tachykinin neurons with several other neuropeptides. For other peptide pairs, the presence of one peptide was not predictive of the presence of the other, and coexpression probability could be replicated by independent probabilities. The stochastic nature of these coexpression patterns highlights the heterogeneity of transmitter content among LNs and argues against clear-cut definition of subpopulation types based on the presence of single neuropeptides. Furthermore, the receptors for all neuropeptides and GABA were expressed within each population of principal neuron type in the antennal lobe (AL). Thus, activation of any given LN results in a dynamic cocktail of modulators that have the potential to influence every level of olfactory processing within the AL.
广泛的神经元类群在许多参数上都出人意料地具有异质性，而且子类通常表现出部分重叠的特征，包括递质共表达。然而，递质共表达是否以可预测、一致的模式发生尚不清楚。在这里，我们证明了鳞翅目昆虫的嗅觉局部中间神经元（LN）中 GABA 和多种神经肽家族的成对共表达具有高度异质性，单个 LN 能够表达至少四个肽家族的神经肽，而很少有神经肽一致共表达的情况。通过计算建模，我们证明了观察到的共表达模式不能用每个神经肽表达的独立概率来解释。我们的分析指出了三个组织原则，一旦考虑到这些原则，就可以复制整体共表达结构：（1）肽能神经元极有可能共表达 GABA；（2）促前胸腺激素的表达概率取决于肌抑制肽的表达；（3）速激肽神经元与其他几种神经肽的全或无共表达模式。对于其他肽对，一种肽的存在并不能预测另一种肽的存在，并且共表达概率可以通过独立概率来复制。这些共表达模式的随机性突出了 LN 中递质含量的异质性，并反对根据单个神经肽的存在来明确定义亚群类型。此外，所有神经肽和 GABA 的受体都在触角叶（AL）中的主要神经元类型的每个群体中表达。因此，任何给定 LN 的激活都会导致动态的调制器混合物，这些调制器有可能影响 AL 内的每个嗅觉处理水平。
