The lamprey blueprint of the mammalian nervous system

The basic features of the vertebrate nervous system are conserved throughout vertebrate phylogeny to a much higher degree than previously thought. In this mini-review, we show that not only the organization of the different motor programs underlying eye, orienting, locomotor, and respiratory movements are similarly organized, but also that the basic structure of the forebrain engaged in the control of movement is conserved. In the lamprey, which diverged already 560 million years ago from the vertebrate line of evolution leading up to primates, the basic components of the basal ganglia are similar to those of mammals in considerable detail. Moreover, the properties of the synaptic input are similar as well as transmitters/peptides in the direct and indirect pathway throughout the basal ganglia. The membrane properties of the striatal projection neurons with D1 and D2 receptors, respectively, are also similar, as are those of the pallidal output neurons. Our evidence suggests that the basal ganglia can be subdivided into functional modules controlling different motor programs, like locomotion and eye movements. What has happened during evolution is that the number of modules has increased in parallel with a progressively more complex behavioral repertoire. For value-based decisions, the circuitry through the lateral habenulae to the dopaminergic modulator neurons is also conserved, as well as the relay inhibitory interneurons involved. The habenular input is from a pallidal glutamatergic nucleus in lamprey as well as mammals, and this nucleus in turn receives input from the striosomal compartment within striatum and also from pallium (cortex in mammals).