Evolutionary origins of chemical synapses.

Synaptic transmission is a fundamental neurobiological process by which neurons interact with each other and non-neuronal cells. It involves release of active substances from the presynaptic neuron onto receptive elements of postsynaptic cells, inducing waves of spreading electrochemical response. While much has been learned about the cellular and molecular mechanisms driving and governing transmitter release and sensing, the evolutionary origin of synaptic connections remains obscure. Herein, we review emerging evidence and concepts suggesting that key components of chemical synapse arose independently from neurons, in different functional and biological contexts, before the rise of multicellular living forms. We argue that throughout evolution, distinct synaptic constituents have been co-opted from ancestral forms for a new role in early metazoan, leading to the rise of chemical synapses and neurotransmission. Such a mosaic model of the origin of chemical synapses agrees with and supports the pluralistic hypothesis of evolutionary change.

Distribution of calcium-binding proteins in the pigeon visual thalamic centers and related pretectal and mesencephalic nuclei. Phylogenetic and functional determinants.

Multichannel processing of environmental information constitutes a fundamental basis of functioning of sensory systems in the vertebrate brain. Two distinct parallel visual systems - the tectofugal and thalamofugal exist in all amniotes. The vertebrate central nervous system contains high concentrations of intracellular calcium-binding proteins (CaBPrs) and each of them has a restricted expression pattern in different brain regions and specific neuronal subpopulations. This study aimed at describing the patterns of distribution of parvalbumin (PV) and calbindin (CB) in the visual thalamic and mesencephalic centers of the pigeon (Columba livia). We used a combination of immunohistochemistry and double labeling immunofluorescent technique. Structures studied included the thalamic relay centers involved in the tectofugal (nucleus rotundus, Rot) and thalamofugal (nucleus geniculatus lateralis, pars dorsalis, GLd) visual pathways as well as pretectal, mesencephalic, isthmic and thalamic structures inducing the driver and/or modulatory action to the visual processing. We showed that neither of these proteins was unique to the Rot or GLd. The Rot contained i) numerous PV-immunoreactive (ir) neurons and a dense neuropil, and ii) a few CB-ir neurons mostly located in the anterior dorsal part and associated with a light neuropil. These latter neurons partially overlapped with the former and some of them colocalized both proteins. The distinct subnuclei of the GLd were also characterized by different patterns of distribution of CaBPrs. Some (nucleus dorsolateralis anterior, pars magnocellularis, DLAmc; pars lateralis, DLL; pars rostrolateralis, DLAlr; nucleus lateralis anterior thalami, LA) contained both CB- and PV-ir neurons in different proportions with a predominance of the former in the DLAmc and DLL. The nucleus lateralis dorsalis of nuclei optici principalis thalami only contained PV-ir neurons and a neuropil similar to the interstitial pretectal/thalamic nuclei of the tectothalamic tract, nucleus pretectalis and thalamic reticular nucleus. The overlapping distribution of PV and CB immunoreactivity was typical for the pretectal nucleus lentiformis mesencephali and the nucleus ectomamillaris as well as for the visual isthmic nuclei. The findings are discussed in the light of the contributive role of the phylogenetic and functional factors determining the circuits׳ specificity of the different CaBPr types.

Wiring prior to firing: the evolutionary rise of electrical and chemical modes of synaptic transmission.

Paracrine signaling and coupling via intercellular conduits are widely utilized for cell-cell interactions from primitive eukaryotes to advanced metazoa. Here, we review the functional and molecular data suggestive of a phylogenic continuum between these primeval forms of communication with the chemical and electrical synaptic transmission of neurons. We discuss selective evidence for the essential role played by the shift of function in early cellular morphologies and protosynaptic scaffolds, with their co-optation for new functionality, which ultimately lead to the rise of the chemical synapse. It is proposed that, rather than representing a transitional element, mixed electrochemical synapses exemplify an exaptive effect. The nonadaptive model of the synaptic origin described herein supports the pluralistic hypothesis of evolutionary change.

Core-and-belt organisation of the mesencephalic and forebrain auditory centres in turtles: expression of calcium-binding proteins and metabolic activity.

The distribution of immunoreactivity to the calcium-binding proteins parvalbumin, calbindin and calretinin and of cytochrome oxidase activity was studied in the mesencephalic (torus semicircularis), thalamic (nucleus reuniens) and telencephalic (ventromedial part of the anterior dorsal ventricular ridge) auditory centres of two chelonian species Emys orbicularis and Testudo horsfieldi. In the torus semicircularis, the central nucleus (core) showed intense parvalbumin immunoreactivity and high cytochrome oxidase activity, whereas the laminar nucleus (belt) showed low cytochrome oxidase activity and dense calbindin/calretinin immunoreactivity. Within the central nucleus, the central and peripheral areas could be distinguished by a higher density of parvalbumin immunoreactivity and cytochrome oxidase activity in the core than in the peripheral area. In the nucleus reuniens, the dorsal and ventromedial (core) regions showed high cytochrome oxidase activity and immunoreactivity to all three calcium-binding proteins, while its ventrolateral part (belt) was weakly immunoreactive and showed lower cytochrome oxidase activity. In the telencephalic auditory centre, on the other hand, no particular region differed in either immunoreactivity or cytochrome oxidase activity. Our findings provide additional arguments in favour of the hypothesis of a core-and-belt organisation of the auditory sensory centres in non-mammalian amniotes though this organisation is less evident in higher order centres. The data are discussed in terms of the evolution of the auditory system in amniotes.

Tectorotundal connections in turtles: an electron microscopic tracing and GABA-immunocytochemical study.

The nucleus rotundus of the turtles Emys orbicularis and Testudo horsfieldi was analysed by axonal tracing methods and post-embedding GABA immunocytochemistry. After injections of horseradish peroxidase or biotinylated dextran amine into the optic tectum, electron microscopic observations showed that the vast majority of ipsilateral tectorotundal axon terminals were small in size, had smooth contours and contained small, round, densely packed synaptic vesicles. These terminals were GABA-immunonegative, often gathered in clusters, and established asymmetrical synaptic contacts with either small- or medium-sized GABA-negative dendritic profiles and with GABA-immunoreactive (GABA-ir) dendrites, which did not contain synaptic vesicles. Occasional GABA-ir-labelled axon terminals were observed; these may arise from the rare GABAergic neurons in the central tectal layer, or from neurons in the ventral pretectal nucleus, which projects both to the optic tectum and nucleus rotundus. In addition to tracer-labelled axon terminals, we observed both GABA-negative and GABA-ir cell bodies and dendrites also labelled by the tracer. No GABA-ir presynaptic dendritic profiles containing synaptic vesicles were observed. The existence in reptiles of reciprocal connections between the nucleus rotundus and the optic tectum as a phylogenetically ancient feedback system is discussed.

Serotonergic modulation of synaptic transmission and action potential firing in frog motoneurons.

Frog spinal neurons receive a prominent innervation from the bulbar serotonergic nuclear complex. We used an isolated spinal cord preparation to examine the effect of serotonin (5-hydroxytryptamine, 5-HT) receptor activation on segmental and descending monosynaptic excitatory inputs to frog lumbar motoneurons. Bath-application of 5-HT (0.05 mM) caused a significant reduction in the peak amplitude of segmental EPSP elicited by dorsal root (DR) stimulation (P < 0.05). Contrasting to DR evoked responses 5-HT did not affect the descending monosynaptic EPSP conditioned by ventrolateral column (VLC) stimulation. Recording of the VLC induced EPSP-spike (E-S) field response within the ventral horn motor nucleus disclosed a substantial enhancement in the population discharge of motoneurons upon 5-HT application (P < 0.05). These data suggest the potential importance of serotonergic receptors in motor integration and gaining of motor output in the frog spinal cord.