Neuronal mechanisms of integrated flight control and goal-directed behaviour in butterfly

稳定姿势的反射是如何与自愿行为相结合的？在运动过程中，包括人类在内的所有动物在各种环境条件下都会保持默认的身体方位。当行走在不平坦的地形上，在湍急的空气中飞行，或在水流中游泳时，强大的内环控制系统不断测量外部扰动并产生负反馈信号来稳定运动。但是，如果一只动物想要改变它的轨迹，比如为了避免碰撞或转向有吸引力的目标，会发生什么？达到这些效果的动作会立即触发反射，稳定原来的身体方向。作为对这个问题的解决方案，冯·霍尔斯特和米特尔斯塔德(1950)提出让动物产生一种“传出副本”，来预测动物对自身产生的动作的感觉反应。传出复制中和了由自主运动引起的“传入”感觉信号，从而防止了稳定反射的影响。使用传出副本的好处是，在意志行为过程中，传出副本不会被完全阻断，而是继续稳定下来，不受不必要的干扰。尽管传出副本被认为有助于脊椎动物和无脊椎动物的感觉处理，但实验证据表明，它们在神经回路中用于运动控制的实验证据最近才在果蝇身上获得。感知广域光流的视觉中间神经元(LPTCs)被发现在苍蝇自愿转向时调节它们的活动，无论是自发的还是对威胁物体的反应。这些调制具有适当的符号和时序，起到传出副本的作用，取消了在一个回合中经历的重新传入信号。然而，目前尚不清楚传出副本是如何针对这些神经元的，传出副本是如何在大脑中计算的，以及它们是否反映了适用于其他行为环境的一般机制。最终，大脑中用于协调行为行动的任何信息都必须传递到身体的运动系统，在昆虫中，这是由下行神经元完成的。在果蝇中，少数下行神经元与LPTCs形成双向突触，并对特定模式的广域光流(WFDN)敏感。WFDN位于胸部的视觉系统和运动系统之间，通过参与产生意志力行为的中央大脑区域，战略性地放置WFDN进行传出复制调制。也有证据表明，在下行神经元的水平上，内环和外环通路之间存在串扰。最近，我们在蝴蝶体内发现了大量的WFDN，这些WFDN可能起到稳定这些生物在不稳定的飞行特性中经历的自我运动的特定成分的功能。蝴蝶是一种敏捷的飞行者，它配备了一个视觉系统，可以根据颜色视觉进行精细调整，在某些物种中，还可以利用各种天窗信号来解决导航外环任务。在这个项目中，我们的目标是了解蝴蝶WFDN中如何整合内环和外环行为。为此，我们将描述蝴蝶WFDN神经生理学和自由飞行运动学之间的关系，并直接探讨它们在拴系飞行的内环和外环行为中的作用。总体而言，该项目将提供概念框架，以促进我们对神经元小电路如何解决昆虫反射陷阱的理解，引导我们走向更具普遍性的集成感觉运动控制的设计原则。

How are reflexes that stabilise posture integrated with voluntary behaviours? During locomotion, all animals, including humans, maintain a default body orientation under various environmental conditions. When walking on uneven terrain, flying in turbulent air, or swimming through water currents, powerful inner-loop control systems constantly measure external perturbations and generate negative feedback signals to stabilise locomotion. But what happens if an animal wants to change its trajectory, for instance to avoid collisions or to turn towards attractive targets? Movements to those effects would immediately trigger reflexes stabilizing the original body orientation. As a result, the animal would be trapped by its own reflexes.As a solution to this problem, von Holst and Mittelstaedt (1950) proposed that animals generate an 'efference copy' that predicts the sensory response to self-generated movements. The efference copy neutralizes 'reafferent' sensory signals caused by the voluntary movement, thus preventing stabilization reflexes from kicking in. The advantage of using efference copies is that rather than being blocked altogether, the inner-loop continues to stabilise against unwanted perturbations during volitional behaviours.Although efference copies have been suggested to aid sensory processing in vertebrates and invertebrates, experimental evidence demonstrating their use in neural circuits for locomotor control was obtained only recently in fruitflies. Visual interneurons sensing wide-field optic flow (LPTCs) were found to modulate their activity whenever the fly made a volitional turn, either spontaneously, or in response to a threatening object. These modulations were of the appropriate sign and timing to function as efference copies, cancelling reafferent signals experienced during a turn. However, it remains unknown how these neurons are targeted by efference copies, how efference copies are calculated within the brain, and whether they reflect a general mechanism applicable for other behavioural contexts.Ultimately, any information in the brain that is used to coordinate behavioural action must be relayed to motor systems in the body, which in insects is done by descending neurons. In flies, a small number of descending neurons form bi-directional synapses with LPTCs and are sensitive to specific patterns of wide-field optic flow (WFDNs). Positioned between the visual system and motor systems in the thorax, WFDNs are strategically placed for efference copy modulation by central brain regions involved in generating volitional behaviour. Evidence is also emerging of crosstalk between inner- and outer-loop pathways at the level of descending neurons. Thus, WFDNs may represent a pathway for efference copy transmission to LPTCs at a more peripheral stage of the sensorimotor pathway.Recently, we have discovered a multitude of WFDNs in the butterfly, which may function to stabilise specific components of self-motion experienced during the erratic flight characteristic of these creatures. Butterflies are agile fliers equipped with a visual system exquisitely tuned to colour vision and, in some species, to solve navigational outer-loop tasks using various skylight cues. In this project, we aim to understand how inner- and outer-loop behaviours are integrated in butterfly WFDNs. To this end we will characterise the relationship between the butterfly WFDN neurophysiology and free-flight kinematics, and directly probe their function during inner- and outer-loop behaviours in tethered flight. Overall, this project will provide the conceptual framework to advance our understanding of how small circuits of neurons solve the reflex trap in insects, leading us towards more generalisable design principles for integrated sensorimotor control.