Elementary nervous systems

Abstract

The evolutionary origin of the nervous system has been a matter of long-standing debate. This is due to the different perspectives taken. Earlier studies addressed nervous system origins at the cellular level. They focused on the selective advantage of the first neuron in its local context, and considered vertical sensory-motor reflex arcs the first nervous system. Later studies emphasized the value of the nervous system at the tissue level. Rather than acting locally, early neurons were seen as part of an elementary nerve net that enabled the horizontal coordination of tissue movements. Opinions have also differed on the nature of effector cells. While most authors have favoured contractile systems, others see the key output of the incipient nervous system in the coordination of motile cilia, or the secretion of antimicrobial peptides. I will discuss these divergent views and explore how they can be validated by molecular and single-cell data. From this survey, possible consensus emerges: (i) the first manifestation of the nervous system likely was a nerve net, whereas specialized local circuits evolved later; (ii) different nerve nets may have evolved for the coordination of contractile or cilia-driven movements; (iii) all evolving nerve nets facilitated new forms of animal behaviour with increasing body size. This article is part of the theme issue 'Basal cognition: multicellularity, neurons and the cognitive lens'.

Keywords: nervous system evolution; nervous system origins; neuron evolution.

Figure 1.

A simplified phylogenetic tree of the animals. Depicted species represent groups of special relevance for comparative neurobiology that are mentioned in the text. The presence of a centralized nervous system in cnidarians and of a brain in ctenophores is discussed in Satterlie [1] and Jager et al. [2]. The branching of the tree follows Kapli & Telford [3].

Figure 2.

Historic views of elementary sensory-effector circuits. (a) Kleinenberg's observation of epithelial muscle cells in Hydra. The first circuit would have evolved via the physical separation of the contractile myofiber from the cell body. Original drawings from Kleinenberg [4]. (b) Parker's three stages of elementary circuit evolution. Original drawings from Parker [6]. (c) Three steps towards the evolution of a simple ciliomotor circuit according to Jékely [11]. (d) A multipolar secretory cell filled with dense core vesicles and multiple extensions as observed in nervous system-less sponges. Redrawn after Lentz [36]. (Online version in colour.)

Figure 3.

Characteristic nerve nets in ctenophores and cnidarians. (a) The polygonal epithelial nerve net of Pleurobrachia pileus redrawn after Jager et al. [45]. (b) The epithelial nerve net of the Hydra polyp from Arendt [53]. (c) Cellular view of the Hydra nerve net. Nerve nets are known to contain stereotypic elements with distinct transmitters [54]. Redrawn after Lentz [50].

Figure 4.

The contractile network hypothesis. (a) Evolutionary precursor state with epithelial mechanosensory and mesenchymal cells with long interconnected contractile and conductive processes forming a tissue-wide network. (b) The first nervous system comprising mechanosensory neurons innervating a tissue-spanning elementary nerve net composed of multipolar interneurons. The nerve net neurons innervate a network of contractile myocytes. Red boxes on the cells represent conductive ion channels. Red lines indicate actomyosin filaments for contraction. (Online version in colour.)

Figure 5.

Locomotor patterns in ancestral metazoans. (a,b) The evolution of nerve-net innervated longitudinal musculature from polarized conductive-contractile cells via division of labour. From Arendt et al. [37]. (c) Interpretative drawing of a Dickinsonia-like animal feeding on organic mats covering the Ediacaran seafloor ('old elephant skin'), following Evans et al. [62] and Ivantsov [63]. Fossil evidence indicates that the animals remained stationary for a period of time, removed the organic mat beneath them via external digestion or ciliary activity, and then moved from that area leaving a depression ('footprint'). Chains of footprints are interpreted as forward movement. Wrinkles on the surface indicate the presence of longitudinal muscles parallel or perpendicular to the gastric pouches (violet and red double arrows), enabling shape change. Locomotor movements may have been cilia- and musculature-driven and controlled by nerve nets.

Figure 6.

Ectomesenchyme in sponges. Interconnected contractile and conductive cells with secretory granules form a mesenchymal network underneath the pinacocyte outer epithelium. Red lines indicate actomyosin fibres. Redrawn and modified after Pavans de Ceccatty [10].

Figure 7.

The neurosecretory network hypothesis. (a) Evolutionary precursor state. Ciliated tissue with equally spaced sensory-neurosecretory cells that secrete neuropeptides. Sensory-neurosecretory cells form numerous basal projections. (b) Elementary nerve net. Horizontal projections of sensory-neurosecretory interconnected via synapses. Synaptic amplification of neurosecretion. Blue circles indicate vesicles of secreted neuropeptides. (Online version in colour.)

Figure 8.

Sensory-neurosecretory cells in the vertebrate brain. Protoneuron-like cells from part of the periventricular ependyme with sensory endings responding to light, ions and flow. Basal neurosecretory processes release vesicles into external body fluids. Reproduced from Vigh et al. [14].