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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

Schematic presentation of magnocellular hypothalamic nuclei in representative examples of basal and advanced vertebrates (drawings are based on Grinevich and Polenov, 1994). 3v, third ventricle; F, columns of fornix; LV, lateral ventricle; MFB, medial forebrain bundle; OC, optic chiasm; OT, optic tract; PON, preoptic nucleus; PVN, paraventricular nucleus; SON, supraoptic nucleus. Accessory nuclei: 1—extrahypothalamic; 2—anterior commissural; 3—circular; 4—fornical; 5—nucleus of the medial forebrain bundle; 6—dorsolateral.
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Figure 1: Schematic presentation of magnocellular hypothalamic nuclei in representative examples of basal and advanced vertebrates (drawings are based on Grinevich and Polenov, 1994). 3v, third ventricle; F, columns of fornix; LV, lateral ventricle; MFB, medial forebrain bundle; OC, optic chiasm; OT, optic tract; PON, preoptic nucleus; PVN, paraventricular nucleus; SON, supraoptic nucleus. Accessory nuclei: 1—extrahypothalamic; 2—anterior commissural; 3—circular; 4—fornical; 5—nucleus of the medial forebrain bundle; 6—dorsolateral.

Mentions: In more basal vertebrates (paraphyletic taxon Anamnia), composed by agnathans, fish and amphibians, magnocellular neurosecretory neurons express homologs of OT (mesotocin, isotocin, glumitocin, valitocin, aspargtocin) and VP (vasotocin) (Acher, 1978; Donaldson and Young, 2008). These neurons reside in the ancestral preoptic nucleus (PON; Diepen, 1962; Figure 1), which became recently a subject of genetic studies, using transgenic fish models (Gutnick et al., 2011; Herget et al., 2013). Magnocellular neurons of adult Anamnia are quite randomly distributed within the PON, existing intermingled with other types of cells. However, there is a ventro-dorsal gradient in size and morphology of neurons—while ventrally located neurons are rather small, more dorsally residing ones are bigger, and neurons reaching the upper pole of the PON are gigantic (Polenov, 1974; Garlov, 2005). This gradient reflects a “physiological regeneration” of the nucleus, which is caused by short periods of increased secretory activity (migration in fish and seasonal changes in frogs) and subsequent death of the gigantic neurosecretory neurons (Polenov, 1974; Garlov, 2005). This cell loss is, hence, compensated by newly born neurons (Chetverukhin and Polenov, 1993; Polenov and Chetverukhin, 1993). Although in non-mammalian species of vertebrates pronounced adult neurogenenesis is reported for various brain regions (see Kaslin et al., 2008 and Refs therein), in mammals this process is rather unique. Here it occurs only in specific areas, such as the subventricular zone and the dentate gyrus of the hippocampus (Ming and Song, 2011) as well as in the peptidergic hypothalamic arcuate nucleus, where cell turnover occurs at a low rate (Kokoeva et al., 2005).


Evolution of oxytocin pathways in the brain of vertebrates.

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

Schematic presentation of magnocellular hypothalamic nuclei in representative examples of basal and advanced vertebrates (drawings are based on Grinevich and Polenov, 1994). 3v, third ventricle; F, columns of fornix; LV, lateral ventricle; MFB, medial forebrain bundle; OC, optic chiasm; OT, optic tract; PON, preoptic nucleus; PVN, paraventricular nucleus; SON, supraoptic nucleus. Accessory nuclei: 1—extrahypothalamic; 2—anterior commissural; 3—circular; 4—fornical; 5—nucleus of the medial forebrain bundle; 6—dorsolateral.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Schematic presentation of magnocellular hypothalamic nuclei in representative examples of basal and advanced vertebrates (drawings are based on Grinevich and Polenov, 1994). 3v, third ventricle; F, columns of fornix; LV, lateral ventricle; MFB, medial forebrain bundle; OC, optic chiasm; OT, optic tract; PON, preoptic nucleus; PVN, paraventricular nucleus; SON, supraoptic nucleus. Accessory nuclei: 1—extrahypothalamic; 2—anterior commissural; 3—circular; 4—fornical; 5—nucleus of the medial forebrain bundle; 6—dorsolateral.
Mentions: In more basal vertebrates (paraphyletic taxon Anamnia), composed by agnathans, fish and amphibians, magnocellular neurosecretory neurons express homologs of OT (mesotocin, isotocin, glumitocin, valitocin, aspargtocin) and VP (vasotocin) (Acher, 1978; Donaldson and Young, 2008). These neurons reside in the ancestral preoptic nucleus (PON; Diepen, 1962; Figure 1), which became recently a subject of genetic studies, using transgenic fish models (Gutnick et al., 2011; Herget et al., 2013). Magnocellular neurons of adult Anamnia are quite randomly distributed within the PON, existing intermingled with other types of cells. However, there is a ventro-dorsal gradient in size and morphology of neurons—while ventrally located neurons are rather small, more dorsally residing ones are bigger, and neurons reaching the upper pole of the PON are gigantic (Polenov, 1974; Garlov, 2005). This gradient reflects a “physiological regeneration” of the nucleus, which is caused by short periods of increased secretory activity (migration in fish and seasonal changes in frogs) and subsequent death of the gigantic neurosecretory neurons (Polenov, 1974; Garlov, 2005). This cell loss is, hence, compensated by newly born neurons (Chetverukhin and Polenov, 1993; Polenov and Chetverukhin, 1993). Although in non-mammalian species of vertebrates pronounced adult neurogenenesis is reported for various brain regions (see Kaslin et al., 2008 and Refs therein), in mammals this process is rather unique. Here it occurs only in specific areas, such as the subventricular zone and the dentate gyrus of the hippocampus (Ming and Song, 2011) as well as in the peptidergic hypothalamic arcuate nucleus, where cell turnover occurs at a low rate (Kokoeva et al., 2005).

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