Dopamine and Octopamine Influence Avoidance Learning of Honey Bees in a Place Preference Assay

Biogenic amines are widely characterized in pathways evaluating reward and punishment, resulting in appropriate aversive or appetitive responses of vertebrates and invertebrates. We utilized the honey bee model and a newly developed spatial avoidance conditioning assay to probe effects of biogenic amines octopamine (OA) and dopamine (DA) on avoidance learning. In this new protocol non-harnessed bees associate a spatial color cue with mild electric shock punishment. After a number of experiences with color and shock the bees no longer enter the compartment associated with punishment. Intrinsic aspects of avoidance conditioning are associated with natural behavior of bees such as punishment (lack of food, explosive pollination mechanisms, danger of predation, heat, etc.) and their association to floral traits or other spatial cues during foraging. The results show that DA reduces the punishment received whereas octopamine OA increases the punishment received. These effects are dose-dependent and specific to the acquisition phase of training. The effects during acquisition are specific as shown in experiments using the antagonists Pimozide and Mianserin for DA and OA receptors, respectively. This study demonstrates the integrative role of biogenic amines in aversive learning in the honey bee as modeled in a novel non-appetitive avoidance learning assay.

生物胺（biogenic amines）在评估奖赏与惩罚的神经通路中被广泛研究，其可介导脊椎动物与无脊椎动物产生适配性的厌恶性与奖赏性应答。本研究以蜜蜂为模式生物，结合全新开发的空间厌恶性条件反射检测体系，探究生物胺章鱼胺（octopamine, OA）与多巴胺（dopamine, DA）对厌恶性学习的调控作用。在该全新实验方案中，未被束缚的蜜蜂会将空间色彩线索与轻度电击惩罚建立关联。经过多次色彩-电击配对训练后，蜜蜂将不再进入与惩罚相关的实验隔间。厌恶性条件反射的内在机制与蜜蜂的自然行为高度契合，例如食物匮乏、爆裂式传粉机制、捕食者威胁、高温等惩罚性场景，以及蜜蜂在觅食过程中将此类惩罚与花部性状或其他空间线索建立关联的行为模式。实验结果显示，多巴胺（DA）会降低蜜蜂所感知到的惩罚强度，而章鱼胺（OA）则会增强其感知到的惩罚强度。此类效应具有剂量依赖性，且仅特异性作用于训练的习得阶段。通过分别靶向多巴胺受体与章鱼胺受体的拮抗剂——匹莫齐特（Pimozide）与米安色林（Mianserin）开展的实验，进一步验证了习得阶段的上述效应具有受体特异性。本研究借助全新的非奖赏性厌恶性学习检测模型，证实了生物胺在蜜蜂厌恶性学习过程中的整合调控作用。