Seyedolmohadesin Maedeh, Fu Xingyang, Torkashvand Mahdi, Rasouli Sina, Lang Samuel, Li Liangzi, Kalinski Cristine, Cook Steven J, Schroeder Frank C, Yemini Eviatar, Venkatachalam Vivek
Department of Physics, Northeastern University, Boston, MA 02115.
Department of Neurobiology, UMass Chan Medical School, Worcester, MA 01655.
bioRxiv. 2025 May 19:2025.05.15.654129. doi: 10.1101/2025.05.15.654129.
Sexually-dimorphic neural circuits play a critical role in shaping sex-specific animal behaviors. Maps of the structural dimorphisms in these circuits have been explored by analyzing "synaptic connectomes", electron micrograph reconstructions of synaptic connectivity. Nevertheless, recent studies in the model organism have shown little to no correlation between the synaptic connectome and dynamic neural activity. Therefore, the extent of sexual dimorphism in functional neural activity remains unknown. To determine the extent of functional sexual-dimorphisms in we compared activity, neuron-by-neuron, across all neurons in the heads of both sexes. To sample a broad view of responses to different sensory modalities, we tested a diverse panel of ethologically-relevant olfactory, gustatory, and chemical stimuli, representing both attractive and aversive cues. We found that nearly every sensory neuron responded dimorphically to at least one cue and monomorphically to other cues, indicating that sexually-dimorphic circuits are pervasive and stimulus dependent. This dimorphic and monomorphic activity was present to a lesser extent in downstream interneurons and even less so in motoneurons, implicating sensory neurons as the primary source and location of sexually-dimorphic activity. Comparing the functional activity we measured to the published synaptic connectomes of both sexes revealed that sexual dimorphism in functional connectivity was distinct from and complementary to sexual dimorphism in synaptic connectivity. Our results provide a first-of-its-kind comparison of whole-brain dynamics between sexes at the level of single neurons, serving as an extensive resource for further investigations of functional sex differences.
性别二态性神经回路在塑造特定性别的动物行为中起着关键作用。通过分析“突触连接组”（突触连接性的电子显微镜重建），对这些回路中的结构二态性图谱进行了探索。然而，在模式生物中的最新研究表明，突触连接组与动态神经活动之间几乎没有相关性。因此，功能性神经活动中的性别二态性程度仍然未知。为了确定功能性性别二态性的程度，我们逐神经元地比较了两性头部所有神经元的活动。为了全面了解对不同感觉模态的反应，我们测试了一系列与行为学相关的嗅觉、味觉和化学刺激，包括吸引性和厌恶性线索。我们发现，几乎每个感觉神经元对至少一种线索有二态性反应，而对其他线索有单态性反应，这表明性别二态性回路普遍存在且依赖于刺激。这种二态性和单态性活动在下游中间神经元中程度较轻，在运动神经元中更轻，这表明感觉神经元是性别二态性活动的主要来源和位置。将我们测量的功能活动与已发表的两性突触连接组进行比较，发现功能连接性中的性别二态性与突触连接性中的性别二态性不同且互补。我们的结果首次在单个神经元水平上对两性之间的全脑动态进行了比较，为进一步研究功能性性别差异提供了丰富的资源。
