RESUMEN
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.
Asunto(s)
Evolución Biológica , Neuronas/fisiología , Transmisión Sináptica/genética , Transmisión Sináptica/fisiología , Animales , Sinapsis/fisiologíaRESUMEN
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.
Asunto(s)
Calbindinas/metabolismo , Columbidae/metabolismo , Mesencéfalo/metabolismo , Parvalbúminas/metabolismo , Tálamo/metabolismo , Animales , Encéfalo/metabolismo , Mapeo Encefálico , Núcleo Celular/metabolismo , Columbidae/genética , Inmunohistoquímica , Neuronas/metabolismo , Filogenia , Área Pretectal/metabolismo , Núcleos Talámicos/metabolismo , Vías VisualesRESUMEN
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.
Asunto(s)
Evolución Biológica , Sinapsis Eléctricas/fisiología , Neuronas/fisiología , Comunicación Paracrina/fisiología , Transmisión Sináptica/fisiología , Animales , Uniones Comunicantes/fisiología , Humanos , Red Nerviosa/fisiologíaRESUMEN
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.
Asunto(s)
Vías Auditivas/metabolismo , Mesencéfalo/metabolismo , Proteínas de Reptiles/metabolismo , Telencéfalo/metabolismo , Tálamo/metabolismo , Tortugas/metabolismo , Animales , Vías Auditivas/enzimología , Calbindina 2 , Calbindinas , Complejo IV de Transporte de Electrones/metabolismo , Inmunohistoquímica , Neuronas/enzimología , Neuronas/metabolismo , Parvalbúminas/metabolismo , Prosencéfalo/enzimología , Prosencéfalo/metabolismo , Proteína G de Unión al Calcio S100/metabolismo , Especificidad de la Especie , Telencéfalo/enzimología , Tálamo/enzimologíaRESUMEN
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.
Asunto(s)
Vías Nerviosas/ultraestructura , Colículos Superiores/ultraestructura , Sinapsis/ultraestructura , Núcleos Talámicos/ultraestructura , Tortugas/anatomía & histología , Ácido gamma-Aminobutírico/metabolismo , Animales , Axones/metabolismo , Axones/ultraestructura , Vías Nerviosas/metabolismo , Colículos Superiores/metabolismo , Sinapsis/metabolismo , Núcleos Talámicos/metabolismo , Tortugas/metabolismoRESUMEN
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.
Asunto(s)
Potenciales de Acción/efectos de los fármacos , Neuronas Motoras/efectos de los fármacos , Serotonina/farmacología , Transmisión Sináptica/efectos de los fármacos , Potenciales de Acción/fisiología , Potenciales de Acción/efectos de la radiación , Animales , Relación Dosis-Respuesta en la Radiación , Estimulación Eléctrica/métodos , Potenciales Postsinápticos Excitadores/efectos de los fármacos , Potenciales Postsinápticos Excitadores/fisiología , Potenciales Postsinápticos Excitadores/efectos de la radiación , Técnicas In Vitro , Neuronas Motoras/fisiología , Neuronas Motoras/efectos de la radiación , Rana ridibunda , Médula Espinal/citología , Transmisión Sináptica/fisiología , Transmisión Sináptica/efectos de la radiaciónRESUMEN
Neurochemical and key connectional characteristics of the anterior entopeduncular nucleus (Enta) of the turtle (Testudo horsfieldi) were studied by axonal tracing techniques and immunohistochemistry of parvalbumin, gamma-aminobutyric acid (GABA) and glutamic acid decarboxylase (GAD). We showed that the Enta, which is located within the dorsal peduncle of the lateral forebrain bundle (Pedd), has roughly topographically organized reciprocal connections with the dorsal thalamic visual nuclei, the nucleus rotundus (Rot) and dorsal lateral geniculate nucleus (GLd). The Enta receives projections from visual telencephalic areas, the anterior dorsal ventricular ridge and dorsolateral cortex/pallial thickening. Most Enta neurons contained GABA and parvalbumin, and some of them were retrogradely labeled when the tracer was injected into the visual dorsal thalamic nuclei. Further experiments using double immunofluorescence revealed colocalization of GAD and parvalbumin in the vast majority of Enta neurons, and many of these cells showed retrograde labeling with Fluoro-gold injected into the Rot and/or GLd. According to these data, the Enta may be considered as a structural substrate for recurrent inhibition of the visual thalamic nuclei. Based on morphological and neurochemical similarity of the turtle Enta, caiman Pedd nucleus, the superior reticular nucleus in birds, and the thalamic reticular nucleus in mammals, we suggest that these structures represent a characteristic component which is common to the thalamic organization in amniotes.
Asunto(s)
Núcleos Talámicos Intralaminares/anatomía & histología , Núcleos Talámicos/anatomía & histología , Tortugas/anatomía & histología , Vías Visuales/anatomía & histología , Caimanes y Cocodrilos/anatomía & histología , Caimanes y Cocodrilos/metabolismo , Animales , Evolución Biológica , Aves/anatomía & histología , Aves/metabolismo , Cuerpos Geniculados/anatomía & histología , Cuerpos Geniculados/metabolismo , Glutamato Descarboxilasa/metabolismo , Inmunohistoquímica , Núcleos Talámicos Intralaminares/metabolismo , Mamíferos/anatomía & histología , Mamíferos/metabolismo , Parvalbúminas/metabolismo , Filogenia , Estilbamidinas , Telencéfalo/anatomía & histología , Telencéfalo/metabolismo , Núcleos Talámicos/metabolismo , Tortugas/metabolismo , Corteza Visual/anatomía & histología , Corteza Visual/metabolismo , Vías Visuales/metabolismo , Ácido gamma-Aminobutírico/metabolismoRESUMEN
The pretectal and tectal projections to the dorsal lateral geniculate nucleus (GLd) of two species of turtle (Emys orbicularis and Testudo horsfieldi) were examined under the electron microscope by using axonal tracing techniques (horseradish peroxidase or biotinylated dextran amine) and postembedding gamma-aminobutyric acid (GABA) immunocytochemistry. After injection of tracer into the pretectum, two types of axon terminals were identified as those of pretectogeniculate pathways. Both contained pleomorphic synaptic vesicles and were more numerous in the inner part of the nucleus. They could be distinguished on the bases of size and shape of their synaptic vesicles, type of synaptic contact, and level of GABA immunoreactivity. One type had a higher density of immunolabeling and established symmetric synaptic contacts, whereas the other, less densely immunolabeled, made asymmetric synaptic contacts. In both cases, synaptic contacts were mainly with relay cells and occasionally with interneurons. We suggest that these two types of pretectogeniculate terminals originate in two separate pretectal nuclei. After injection of tracer into the optic tectum, a single population of GABA-immunonegative tracer-labeled terminals was identified as belonging to the tectogeniculate pathway. These were small, had smooth contours, contained very small round synaptic vesicles, and established asymmetric synaptic contacts with long active zones, predominantly with relay cells and less frequently with interneurons, in the inner part of the nucleus. In addition, a population of GABA-negative and occasionally GABA-positive terminals, labeled by tracer injected into either the pretectum or the tectum, was identified as retinal terminals; these were presumably labeled by the retrograde transport of tracer in collateral branches of visual fibers innervating both the GLd and the pretectum or tectum. Comparison of the present ultrastructural findings in turtles with those previously reported in mammals shows that the cytological features, synaptic morphology, and immunochemical properties of the pretectogeniculate and tectogeniculate terminals of both groups share many similarities. Nevertheless, the postsynaptic targets of these two categories of terminals display some pronounced differences between the two groups, which are discussed in terms of their possible functional significance.
Asunto(s)
Axones/ultraestructura , Cuerpos Geniculados/ultraestructura , Colículos Superiores/ultraestructura , Tortugas/anatomía & histología , Tortugas/fisiología , Ácido gamma-Aminobutírico/análisis , Vías Aferentes/química , Vías Aferentes/ultraestructura , Animales , Axones/química , Cuerpos Geniculados/química , Colículos Superiores/químicaRESUMEN
In two species of turtle (Emys orbicularis and Testudo horsfieldi), retrograde and anterograde tracer techniques were used to study projections from the optic tectum to the nucleus rotundus (Rot) and to the dorsal lateral geniculate nucleus (GLd). The ipsilateral Rot received the most massive tectal projections, stemming from numerous neurons located in the stratum griseum centrale (SGC). These neurons varied in size and shape, many of them having a wide zone of dendritic arborization within both the (SGC) and the stratum griseum et fibrosum superficiale (SGFS). Projections from the tectum to the GLd were ipsilateral, were extremely scarce, and arose from a small number of neurons of various shapes situated in the SGFS; these cells were, as a rule, smaller than those projecting to the Rot. For the most part, these neurons were radially oriented, with rather restricted dendritic arborizations in the most superficial sublayers of the SGFS; smaller numbers of projection neurons were horizontally oriented, with long dendrites branching throughout the layer. Some neurons located in the stratum griseum periventriculare (SGP) projected to both the Rot and the GLd. Most of these neurons had dendritic arborizations within the retinorecipient zone of the SGFS. We were unable to rule out the possibility that some cells projecting to the GLd were situated in the SGC. Both the GLd and the main body of the Rot did not contain neurons projecting to the optic tectum. Thalamic neurons projecting to the tectum were observed in the ventral lateral geniculate nucleus, the intergeniculate leaflet and the interstitial nuclei of the tectothalamic tract, and the nucleus of the decussatio supraoptica ventralis. The question of whether variation in the laminar organization of the tectorotundal and tectogeniculate projection neurons in reptiles, birds, and mammals may be related to different degrees of differentiation of the tectal layers is discussed.