Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA.
Proc Biol Sci. 2024 Jan 31;291(2015):20232172. doi: 10.1098/rspb.2023.2172.
The evolution of flight is a rare event in vertebrate history, and one that demands functional integration across multiple anatomical/physiological systems. The neuroanatomical basis for such integration and the role that brain evolution assumes in behavioural transformations remain poorly understood. We make progress by (i) generating a positron emission tomography (PET)-based map of brain activity for pigeons during rest and flight, (ii) using these maps in a functional analysis of the brain during flight, and (iii) interpreting these data within a macroevolutionary context shaped by non-avian dinosaurs. Although neural activity is generally conserved from rest to flight, we found significant increases in the cerebellum as a whole and optic flow pathways. Conserved activity suggests processing of self-movement and image stabilization are critical when a bird takes to the air, while increased visual and cerebellar activity reflects the importance of integrating multimodal sensory information for flight-related movements. A derived cerebellar capability likely arose at the base of maniraptoran dinosaurs, where volumetric expansion and possible folding directly preceded paravian flight. These data represent an important step toward establishing how the brain of modern birds supports their unique behavioural repertoire and provide novel insights into the neurobiology of the bird-like dinosaurs that first achieved powered flight.
飞行的进化在脊椎动物历史上是罕见的事件，需要多个解剖/生理系统的功能整合。这种整合的神经解剖学基础以及大脑进化在行为转变中所起的作用仍知之甚少。我们通过以下方式取得进展：(i) 在鸽子休息和飞行期间生成基于正电子发射断层扫描（PET）的大脑活动图谱，(ii) 在飞行期间使用这些图谱进行大脑的功能分析，以及 (iii) 在由非鸟类恐龙塑造的宏观进化背景下解释这些数据。尽管从休息到飞行时神经活动通常是保守的，但我们发现整个小脑和光流通路的活动显著增加。保守的活动表明，当鸟类飞向天空时，处理自身运动和图像稳定是至关重要的，而增加的视觉和小脑活动反映了为与飞行相关的运动整合多模态感觉信息的重要性。衍生的小脑能力可能起源于手盗龙类恐龙的基部，那里的体积扩张和可能的折叠直接发生在虚骨龙类飞行之前。这些数据代表了朝着确定现代鸟类的大脑如何支持其独特的行为组合迈出的重要一步，并为首次实现动力飞行的类似鸟类的恐龙的神经生物学提供了新的见解。
