Origin and early evolution of neural circuits for the control of ciliary locomotion

Abstract

Behaviour evolved before nervous systems. Various single-celled eukaryotes (protists) and the ciliated larvae of sponges devoid of neurons can display sophisticated behaviours, including phototaxis, gravitaxis or chemotaxis. In single-celled eukaryotes, sensory inputs directly influence the motor behaviour of the cell. In swimming sponge larvae, sensory cells influence the activity of cilia on the same cell, thereby steering the multicellular larva. In these organisms, the efficiency of sensory-to-motor transformation (defined as the ratio of sensory cells to total cell number) is low. With the advent of neurons, signal amplification and fast, long-range communication between sensory and motor cells became possible. This may have first occurred in a ciliated swimming stage of the first eumetazoans. The first axons may have had en passant synaptic contacts to several ciliated cells to improve the efficiency of sensory-to-motor transformation, thereby allowing a reduction in the number of sensory cells tuned for the same input. This could have allowed the diversification of sensory modalities and of the behavioural repertoire. I propose that the first nervous systems consisted of combined sensory-motor neurons, directly translating sensory input into motor output on locomotor ciliated cells and steering muscle cells. Neuronal circuitry with low levels of integration has been retained in cnidarians and in the ciliated larvae of some marine invertebrates. This parallel processing stage could have been the starting point for the evolution of more integrated circuits performing the first complex computations such as persistence or coincidence detection. The sensory-motor nervous systems of cnidarians and ciliated larvae of diverse phyla show that brains, like all biological structures, are not irreducibly complex.

Figure 1.

Comparison of the efficiency of sensory-to-motor transformation in (a) Chlamydomonas, (b) Volvox, (c) a sponge larva, and (d) an annelid larva. The parts of the organism involved in sensing and responding to the light stimulus are coloured red.

Figure 2.

(a) Evolution of the first neurons to control ciliary locomotion from a sensory cell regulating its neighbouring cells by paracrine signals or (b) producing a cell-autonomous motor output with its cilia. (c) The evolution of long-range axonal contact of sensory cells to ciliated motor cells allowed the reduction of cells specialized in one input. This price reduction in sensing and behaviour allowed an increase in the number of senses.

Figure 3.

(a) Comparison of ciliary swimmers with monociliated cells and (b) multiciliated cells. The concentration of cilia in multiciliated cells allows a further reduction in the number of sensory cells required for one external input.

Figure 4.

(a) Evolution of muscle-controlling sensory-motor neurons from a myoepithelial cell by cell-type duplication and divergence. Originally, the motor control of muscles and cilia may have been linked in a ciliary swimming and muscle-based turning circuit. The integration of signals from more sensory cells evolved as some cells migrated deeper in the tissue (shown in red) and collected inputs from their sister cell type on the surface. The first dendrites could have evolved from the ‘sensory synapse’. (b) Evolution of a sign-reversing circuit by cell-type duplication and the segregation of an activatory and inhibitory transmitter. The circuit triggers the contraction of the longitudinal muscles and the relaxation of the circular muscles.