The pretectal connectome in lamprey.

In vertebrates, the pretectum and optic tectum (superior colliculus in mammals) are visuomotor areas that process sensory information and shape motor responses. Whereas the tectum has been investigated in great detail, the pretectum has received far less attention. The present study provides a detailed analysis of the connectivity and neuronal properties of lamprey pretectal cells. The pretectum can be subdivided roughly into three areas based on cellular location and projection pattern: superficial, central, and periventricular. Three different types of pretectal cells could be distinguished based on neuronal firing patterns. One type, the rapid spike-inactivation cells, preferentially lie within the periventricular zone; the other cell types are distributed more generally. In terms of afferentation, the pretectum receives electro- and mechanoreceptive inputs in addition to retinal input. Histological data reveal that a large number of pretectal cells in the superficial and central areas extend dendrites into the optic tract, suggesting a predominant retinal influence even outside of the normal retinal terminal areas. The pretectum receives inhibitory input from the basal ganglia, and input from the pallium (cortex in mammals) and torus semicircularis. In addition, the pretectum is reciprocally connected with the thalamus, tectum, octavolateral area, and habenula. The main pretectal output is to the reticulospinal nuclei, and thus the pretectum indirectly affects the control of movement. Efference copies of some of this output are relayed to the thalamus and tectum. Overall, its extensive circuitry-especially the reciprocal connectivity with other retinorecipient areas-underlines the importance of the pretectum for sensory integration and visuomotor functions. J. Comp. Neurol. 525:753-772, 2017. © 2016 Wiley Periodicals, Inc.

The lamprey pallium provides a blueprint of the mammalian motor projections from cortex.

BACKGROUND: The frontal lobe control of movement in mammals has been thought to be a specific function primarily related to the layered neocortex with its efferent connections. In contrast, we now show that the same basic organization is present even in one of the phylogenetically oldest vertebrates, the lamprey. RESULTS: Stimulation of specific sites in the pallium/cortex evokes eye, trunk, locomotor, or oral movements. The pallial projection neurons target brainstem motor centers and basal ganglia subnuclei and have prominent dendrites extending into the outer molecular layer. They exhibit the characteristic features of pyramidal neurons and elicit monosynaptic glutamatergic excitatory postsynaptic potentials in output neurons of the optic tectum, reticulospinal neurons, and, as shown earlier, basal ganglia neurons. CONCLUSIONS: Our results demonstrate marked similarities in the efferent functional connectivity and control of motor behavior between the lamprey pallium and mammalian neocortex. Thus, the lamprey motor pallium/cortex represents an evolutionary blueprint of the corresponding mammalian system.

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).