Ultrastructure of synapses in the first-evolved nervous systems

Abstract

The phylum Cnidaria represents the first group of animals to evolve a recognizable nervous system. A comparison of the ultrastructural features of synaptic loci in animals representing all four classes of the cnidaria has provided an overview of the first-evolved synapses that can be compared morphologically to synapses in higher forms. Synapses in these watery jellylike animals with unmyelinated axons are sparse and difficult to fix well. However, we now have sufficient evidence to define an early synapse as one with paired electron dense plasma membranes separated by a 13-25 nm gap containing intracleft filaments and with vesicles on one or both sides of the synaptic cleft. The vesicles are of three types: dense-cored, clear, and opaque. Neuromuscular synapses resemble neuronal synapses and lack the postsynaptic specializations of higher animals. However, some coelenterates, such as the jellyfish Chrysaora, have a postsynaptic cisterna in the muscle. Neuromuscular and neuronematocyte synapses can have either clear or dense-cored vesicles. Opaque vesicles at two-way interneuronal synapses and at neuromuscular synapses in the oral sphincter muscle of sea anemones can be labelled with antisera to the neuropeptides Antho-RFamide (Antho-Arg-Phe-NH2) and Antho-RWamides (Antho-Arg-Trp-NH2) I and II, respectively. That suggests that neuropeptides evolved as neurotransmitters early in the animal kingdom. The basic differences between first evolved synapses and synapses of higher animals are the lack of postjunctional folds at neuromuscular synapses and the presence of fewer and somewhat larger synaptic vesicles, generally containing granular cores, in the more primitive animals.

Peptide-gated ion channels and the simple nervous system of Hydra

“…2) (Westfall et al, 1971;Westfall, 1973). These clear vesicles might represent dense-cored vesicles that have lost their cores during neurotransmission (Westfall, 1996). A neuron may synapse more than once with the same epitheliomuscular cell or with two different Peptide-gated ion channels and the simple nervous system of Hydra Stefan Gründer* and Marc Assmann epitheliomuscular cells (Westfall, 1973).…”

“…In addition, the neuromuscular junction of Hydra lacks postsynaptic folds that are characteristic of the neuromuscular junction in higher animals ( Fig. 2) (Westfall, 1996).…”

Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa)

“…There is now ample evidence that the 'simplicity' of the cnidarian nervous net does not occur at the cellular level but rather in the organisation of conducting systems (Kass-Simon and Pierobon, 2007). Cnidarian neurons, in fact, are electrically excitable, show the typical extended morphology and are connected by chemical synapses, gap junctions or syncytial bridges (Jha and Mackie, 1967;Filshie and Flower, 1977;Wood, 1979;Westfall, 1987Westfall, , 1996Holtman and Thurm, 2001). They produce Na + -dependent action potentials, interact by chemical or electrical synapses with other neurons or with nematocytes, muscle processes and other effector cells, generate rhythmic electrical activity and coordinate responses to sensory stimulation, integrating information from a variety of conduction pathways (Anderson, 2004).…”

“…The seminal work by Jane Westfall and coworkers, who described in detail the ultrastructure of nerve cells and synapses in Hydra sp. and other coelenterates contributed to definitely establish the presence of synaptic connections in the following years, erasing residual doubts on the existence of a nervous system (Westfall, 1970(Westfall, , 1973a(Westfall, , 1973b(Westfall, , 1988(Westfall, , 1996(Westfall, , 2002; see also Kass-Simon and Pierobon, 2007 for review).…”

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

“…1). Thanks to their nervous system, cnidarians are the simplest organisms in which movements are governed by a neuromuscular system Westfall (1996), specially their active feeding behavior, which rely on coordinated movements of their tentacles. In contrast, poriferans (sponges), which diverged earlier during evolution, feed by passive filtration.…”