Department of Neurobiology, Harvard Medical School, Boston, MA, USA.
Nature. 2019 Dec;576(7785):121-125. doi: 10.1038/s41586-019-1772-4. Epub 2019 Nov 20.
In the Drosophila brain, 'compass' neurons track the orientation of the body and head (the fly's heading) during navigation . In the absence of visual cues, the compass neuron network estimates heading by integrating self-movement signals over time. When a visual cue is present, the estimate of the network is more accurate. Visual inputs to compass neurons are thought to originate from inhibitory neurons called R neurons (also known as ring neurons); the receptive fields of R neurons tile visual space. The axon of each R neuron overlaps with the dendrites of every compass neuron, raising the question of how visual cues are integrated into the compass. Here, using in vivo whole-cell recordings, we show that a visual cue can evoke synaptic inhibition in compass neurons and that R neurons mediate this inhibition. Each compass neuron is inhibited only by specific visual cue positions, indicating that many potential connections from R neurons onto compass neurons are actually weak or silent. We also show that the pattern of visually evoked inhibition can reorganize over minutes as the fly explores an altered virtual-reality environment. Using ensemble calcium imaging, we demonstrate that this reorganization causes persistent changes in the compass coordinate frame. Taken together, our data suggest a model in which correlated pre- and postsynaptic activity triggers associative long-term synaptic depression of visually evoked inhibition in compass neurons. Our findings provide evidence for the theoretical proposal that associative plasticity of sensory inputs, when combined with attractor dynamics, can reconcile self-movement information with changing external cues to generate a coherent sense of direction.
在果蝇的大脑中，“指南针”神经元在导航过程中跟踪身体和头部（即苍蝇的头部）的方向。在没有视觉线索的情况下，指南针神经元网络通过随时间整合自身运动信号来估计航向。当存在视觉线索时，网络的估计会更准确。人们认为，指南针神经元的视觉输入来自称为 R 神经元（也称为环神经元）的抑制性神经元；R 神经元的感受野覆盖视觉空间。每个 R 神经元的轴突与每个指南针神经元的树突重叠，这就提出了一个问题，即视觉线索如何整合到指南针中。在这里，我们使用体内全细胞记录，表明视觉线索可以在指南针神经元中引发突触抑制，而 R 神经元介导这种抑制。每个指南针神经元仅被特定的视觉线索位置抑制，这表明 R 神经元与指南针神经元之间有许多潜在的连接实际上很弱或沉默。我们还表明，随着苍蝇探索改变的虚拟现实环境，视觉诱发抑制的模式可以在几分钟内重新组织。使用集合钙成像，我们证明这种重组会导致指南针坐标框架中持续发生变化。总的来说，我们的数据表明，在模型中，相关的突触前和突触后活动可以触发指南针神经元中视觉诱发抑制的联想长时程突触抑制，从而为理论建议提供了证据，即感觉输入的联想可塑性与吸引子动力学相结合，可以协调自身运动信息与不断变化的外部线索，从而产生连贯的方向感。
