Limits...
Evolution of oxytocin pathways in the brain of vertebrates.

Knobloch HS, Grinevich V - Front Behav Neurosci (2014)

Bottom Line: Due to these microanatomical and cytological changes, the ancient release modes of oxytocin into the cerebrospinal fluid were largely replaced by vascular release.Furthermore, we draw attention to the non-synaptic axonal release in small and defined brain regions with the aim to clearly distinguish this way of oxytocin action from the classical synaptic transmission on one side and from dendritic release followed by a global diffusion on the other side.Finally, we will summarize the effects of oxytocin and its homologs on pro-social reproductive behaviors in representatives of the phylogenetic tree and will propose anatomically plausible pathways of oxytocin release contributing to these behaviors in basal vertebrates and amniots.

View Article: PubMed Central - PubMed

Affiliation: Schaller Research Group on Neuropeptides, German Cancer Research Center (DKFZ), Max Planck Institute for Medical Research, University of Heidelberg Heidelberg, Germany.

ABSTRACT
The central oxytocin system transformed tremendously during the evolution, thereby adapting to the expanding properties of species. In more basal vertebrates (paraphyletic taxon Anamnia, which includes agnathans, fish and amphibians), magnocellular neurosecretory neurons producing homologs of oxytocin reside in the wall of the third ventricle of the hypothalamus composing a single hypothalamic structure, the preoptic nucleus. This nucleus further diverged in advanced vertebrates (monophyletic taxon Amniota, which includes reptiles, birds, and mammals) into the paraventricular and supraoptic nuclei with accessory nuclei (AN) between them. The individual magnocellular neurons underwent a process of transformation from primitive uni- or bipolar neurons into highly differentiated neurons. Due to these microanatomical and cytological changes, the ancient release modes of oxytocin into the cerebrospinal fluid were largely replaced by vascular release. However, the most fascinating feature of the progressive transformations of the oxytocin system has been the expansion of oxytocin axonal projections to forebrain regions. In the present review we provide a background on these evolutionary advancements. Furthermore, we draw attention to the non-synaptic axonal release in small and defined brain regions with the aim to clearly distinguish this way of oxytocin action from the classical synaptic transmission on one side and from dendritic release followed by a global diffusion on the other side. Finally, we will summarize the effects of oxytocin and its homologs on pro-social reproductive behaviors in representatives of the phylogenetic tree and will propose anatomically plausible pathways of oxytocin release contributing to these behaviors in basal vertebrates and amniots.

No MeSH data available.


Related in: MedlinePlus

Contacts of OT neurons and respective routes of OT release in the brain of basal and advanced vertebrates. 1—dendro-ventricular contacts (trans-ventricular route of OT action); 2—axo-vasal contacts (release into systemic blood circulation); 3—axo-adenar contacts (paracrine action on adenotrophes); 4—axovasal contacts with portal venes; 5—dendritic release; 6—axonal release. 3v, third ventricle; PV, portal vessels.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3924577&req=5

Figure 3: Contacts of OT neurons and respective routes of OT release in the brain of basal and advanced vertebrates. 1—dendro-ventricular contacts (trans-ventricular route of OT action); 2—axo-vasal contacts (release into systemic blood circulation); 3—axo-adenar contacts (paracrine action on adenotrophes); 4—axovasal contacts with portal venes; 5—dendritic release; 6—axonal release. 3v, third ventricle; PV, portal vessels.

Mentions: Like probably many other neuronal cell types (Arendt, 2008), the hypothalamic magnocellular neurons underwent tremendous modifications in term of location and cytological organization during evolution (Polenov, 1978; Scharrer, 1978). The most primitive neurosecretory neurons were observed in Amphioxus (lancelet) (Obermüller-Wilén, 1979), which split from vertebrate ancestors ~550 million years ago (Gee, 2008; Figure 3). In Amphioxus, the neurosecretory cell bodies are lying between the ependymal cells and extend their axonal process through the inner wall of the ventricle to the ventral brain surface (Obermüller-Wilén, 1979). In fish, especially in the basal members of Actinopterygii (ray-finned fish) (e.g., sturgeon, sterlet), the cells extend their dendrites with expanded terminal parts into the lumen of the ventricle while their axons run away from the ventricle roughly at 90° angle. In addition, it seems that in Anamnia these dendrites are not only capable to release neuropeptides into the lumen of the third ventricle but also may sense (at least in the case of vasotocin neurons) via cilia the chemical content of the cerebro-spinal fluid (CSF, Tessmar-Raible et al., 2007). In mammals, a portion of these ventricle contacts seem to remain: using viral based technique the location of OT fibers (axons and/or dendrites) could be shown in intimate proximity to the 3rd ventricle and even in between of ependymal cells, contacting directly with the CSF (Figure 4C). Further along the phylogenic tree (see Figure 2) the majority dendrites and cell bodies of magnocellular neurons move away from the 3rd ventricle and undergo “neuronalization”4 forming rich dendritic trees and unique axonal specializations (the latter is described in great details in sections below). In respect of progressive changes of dendritic trees in evolution, it should be mentioned here that even in mammals (rats, dogs and monkeys) a fraction of OT neurons carries features of relatively simply organized neurons (Hatton, 1990; Armstrong, 1995; and references therein). These cells, visualized by Golgi (silver impregnation) technique, mostly reside in the SON, representing about half of neuronal population in this nucleus. They are bipolar neurons, similar to those observed in basal vertebrates, fish and frogs, while another half of SON neurons are multipolar cells with elaborated dendritic trees (Hatton, 1990; Armstrong, 1995, 2004; and references therein). The number of spines (as well as synapses) on dendrites of OT neurons is relatively modest (~500–600 synapses per OT neuron; William Armstrong, personal communication) especially compared to principle neurons of hippocampus (~10,000 synapses per single CA1 or CA3 neuron; Megias et al., 2001; Hosseini-Sharifabad and Nyengaard, 2007). However, during maternity period OT neurons undergo plastic changes (swelling, arborization) with ultrastructural reorganization of synaptic contacts (Stern and Armstrong, 1998; Theodosis and Poulain, 2001).


Evolution of oxytocin pathways in the brain of vertebrates.

Knobloch HS, Grinevich V - Front Behav Neurosci (2014)

Contacts of OT neurons and respective routes of OT release in the brain of basal and advanced vertebrates. 1—dendro-ventricular contacts (trans-ventricular route of OT action); 2—axo-vasal contacts (release into systemic blood circulation); 3—axo-adenar contacts (paracrine action on adenotrophes); 4—axovasal contacts with portal venes; 5—dendritic release; 6—axonal release. 3v, third ventricle; PV, portal vessels.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3924577&req=5

Figure 3: Contacts of OT neurons and respective routes of OT release in the brain of basal and advanced vertebrates. 1—dendro-ventricular contacts (trans-ventricular route of OT action); 2—axo-vasal contacts (release into systemic blood circulation); 3—axo-adenar contacts (paracrine action on adenotrophes); 4—axovasal contacts with portal venes; 5—dendritic release; 6—axonal release. 3v, third ventricle; PV, portal vessels.
Mentions: Like probably many other neuronal cell types (Arendt, 2008), the hypothalamic magnocellular neurons underwent tremendous modifications in term of location and cytological organization during evolution (Polenov, 1978; Scharrer, 1978). The most primitive neurosecretory neurons were observed in Amphioxus (lancelet) (Obermüller-Wilén, 1979), which split from vertebrate ancestors ~550 million years ago (Gee, 2008; Figure 3). In Amphioxus, the neurosecretory cell bodies are lying between the ependymal cells and extend their axonal process through the inner wall of the ventricle to the ventral brain surface (Obermüller-Wilén, 1979). In fish, especially in the basal members of Actinopterygii (ray-finned fish) (e.g., sturgeon, sterlet), the cells extend their dendrites with expanded terminal parts into the lumen of the ventricle while their axons run away from the ventricle roughly at 90° angle. In addition, it seems that in Anamnia these dendrites are not only capable to release neuropeptides into the lumen of the third ventricle but also may sense (at least in the case of vasotocin neurons) via cilia the chemical content of the cerebro-spinal fluid (CSF, Tessmar-Raible et al., 2007). In mammals, a portion of these ventricle contacts seem to remain: using viral based technique the location of OT fibers (axons and/or dendrites) could be shown in intimate proximity to the 3rd ventricle and even in between of ependymal cells, contacting directly with the CSF (Figure 4C). Further along the phylogenic tree (see Figure 2) the majority dendrites and cell bodies of magnocellular neurons move away from the 3rd ventricle and undergo “neuronalization”4 forming rich dendritic trees and unique axonal specializations (the latter is described in great details in sections below). In respect of progressive changes of dendritic trees in evolution, it should be mentioned here that even in mammals (rats, dogs and monkeys) a fraction of OT neurons carries features of relatively simply organized neurons (Hatton, 1990; Armstrong, 1995; and references therein). These cells, visualized by Golgi (silver impregnation) technique, mostly reside in the SON, representing about half of neuronal population in this nucleus. They are bipolar neurons, similar to those observed in basal vertebrates, fish and frogs, while another half of SON neurons are multipolar cells with elaborated dendritic trees (Hatton, 1990; Armstrong, 1995, 2004; and references therein). The number of spines (as well as synapses) on dendrites of OT neurons is relatively modest (~500–600 synapses per OT neuron; William Armstrong, personal communication) especially compared to principle neurons of hippocampus (~10,000 synapses per single CA1 or CA3 neuron; Megias et al., 2001; Hosseini-Sharifabad and Nyengaard, 2007). However, during maternity period OT neurons undergo plastic changes (swelling, arborization) with ultrastructural reorganization of synaptic contacts (Stern and Armstrong, 1998; Theodosis and Poulain, 2001).

Bottom Line: Due to these microanatomical and cytological changes, the ancient release modes of oxytocin into the cerebrospinal fluid were largely replaced by vascular release.Furthermore, we draw attention to the non-synaptic axonal release in small and defined brain regions with the aim to clearly distinguish this way of oxytocin action from the classical synaptic transmission on one side and from dendritic release followed by a global diffusion on the other side.Finally, we will summarize the effects of oxytocin and its homologs on pro-social reproductive behaviors in representatives of the phylogenetic tree and will propose anatomically plausible pathways of oxytocin release contributing to these behaviors in basal vertebrates and amniots.

View Article: PubMed Central - PubMed

Affiliation: Schaller Research Group on Neuropeptides, German Cancer Research Center (DKFZ), Max Planck Institute for Medical Research, University of Heidelberg Heidelberg, Germany.

ABSTRACT
The central oxytocin system transformed tremendously during the evolution, thereby adapting to the expanding properties of species. In more basal vertebrates (paraphyletic taxon Anamnia, which includes agnathans, fish and amphibians), magnocellular neurosecretory neurons producing homologs of oxytocin reside in the wall of the third ventricle of the hypothalamus composing a single hypothalamic structure, the preoptic nucleus. This nucleus further diverged in advanced vertebrates (monophyletic taxon Amniota, which includes reptiles, birds, and mammals) into the paraventricular and supraoptic nuclei with accessory nuclei (AN) between them. The individual magnocellular neurons underwent a process of transformation from primitive uni- or bipolar neurons into highly differentiated neurons. Due to these microanatomical and cytological changes, the ancient release modes of oxytocin into the cerebrospinal fluid were largely replaced by vascular release. However, the most fascinating feature of the progressive transformations of the oxytocin system has been the expansion of oxytocin axonal projections to forebrain regions. In the present review we provide a background on these evolutionary advancements. Furthermore, we draw attention to the non-synaptic axonal release in small and defined brain regions with the aim to clearly distinguish this way of oxytocin action from the classical synaptic transmission on one side and from dendritic release followed by a global diffusion on the other side. Finally, we will summarize the effects of oxytocin and its homologs on pro-social reproductive behaviors in representatives of the phylogenetic tree and will propose anatomically plausible pathways of oxytocin release contributing to these behaviors in basal vertebrates and amniots.

No MeSH data available.


Related in: MedlinePlus