Ancestral regulatory mechanisms specify conserved midbrain circuitry in arthropods and vertebrates

Abstract

Corresponding attributes of neural development and function suggest arthropod and vertebrate brains may have an evolutionarily conserved organization. However, the underlying mechanisms have remained elusive. Here, we identify a gene regulatory and character identity network defining the deutocerebral–tritocerebral boundary (DTB) in Drosophila. This network comprises genes homologous to those directing midbrain-hindbrain boundary (MHB) formation in vertebrates and their closest chordate relatives. Genetic tracing reveals that the embryonic DTB gives rise to adult midbrain circuits that in flies control auditory and vestibular information processing and motor coordination, as do MHB-derived circuits in vertebrates. DTB-specific gene expression and function are directed by cis-regulatory elements of developmental control genes that include homologs of mammalian Zinc finger of the cerebellum and Purkinje cell protein 4. Drosophila DTB-specific cis-regulatory elements correspond to regulatory sequences of human ENGRAILED-2, PAX-2, and DACHSHUND-1 that direct MHB-specific expression in the embryonic mouse brain. We show that cis-regulatory elements and the gene networks they regulate direct the formation and function of midbrain circuits for balance and motor coordination in insects and mammals. Regulatory mechanisms mediating the genetic specification of cephalic neural circuits in arthropods correspond to those in chordates, thereby implying their origin before the divergence of deuterostomes and ecdysozoans.

Shore crabs reveal novel evolutionary attributes of the mushroom body

“…However, mushroom bodies are situated rostral to the arthropod brain’s deutocerebral-tritocerebral boundary. A homologous location is occupied by the hippocampi, rostral to the vertebrate midbrain-hindbrain boundary ( Bridi et al, 2020 ). Mushroom bodies and hippocampi are restricted, respectively, to the protocerebrum and its vertebrate homologue the telencephalon ( Hirth and Reichert, 1999 ).…”

How Asymmetries Evolved: Hearts, Brains, and Molecules

“…The dorsal-ventral axis evolved later through the influence of gravity and the demands of locomotion, creating consistent differences between top and bottom, such as eyes placed high for distance vision and feet touching the ground. The formation of these two axes, with their distinctive asymmetries, appears to be highly conserved genetically, at least across vertebrates and arthropods [3].…”

The lower Cambrian lobopodian Cardiodictyon resolves the origin of euarthropod brains

“…Only in crown Euarthropoda is there an embryonic contribution to the brain from the first metameric trunk ganglion, which migrates forward to become the tritocerebrum, contiguous with the deutocerebrum. The deuto- and tritocerebral interface defines the boundary between the mid- and hindbrain ( 47 ), thus marking the point of coalescence of two connected but genetically and evolutionarily distinct components of the nervous system.…”