Head direction and the evolutionary origins of spatial representation

Spatial representations are a fundamental aspect of cognition. It remains largely unknown when and why the capacity to neurally represent space first evolved. In this opinion article, we argue that a strong candidate for the earliest such representation is the encoding of head direction. Dedicated circuits that compute head direction by integrating self-motion and external cues have been described in both vertebrates and insects and are likely to be ancestral in each lineage. This suggests a Cambrian or possibly Precambrian origin for head direction representation. In both lineages, head direction circuits occupy an evolutionarily and functionally foundational position. They occur in deeply conserved brain structures, sit upstream of other spatial representations, and can emerge from minimal neural architecture. In mammals, they also develop before other spatial systems. Together, these features suggest that head direction was the first neural representation of space, offering a window into the evolution of neural representation and spatial cognition more generally.