Abstract
The organization of the pallial derivatives across vertebrates follows a comparable elementary arrangement, although not all of them possess a layered cortical structure as sophisticated as the cerebral cortex of mammals. However, its expansion along evolution has only been possible by the development and coevolution of the cellular networks formed by excitatory neurons and inhibitory interneurons. Thus, the comparative analysis of interneuron types in vertebrate models of key evolutionary significance will provide important information, due to the extraordinary anatomical sophistication of their interneuron systems with simpler behavioral implications. Particularly in mammals, the main consensus for classifying interneuron types is based on non-overlapping markers, which do not form a single population, but consist of several distinct classes of inhibitory cells showing co-expression of other markers. In our study, we analyzed immunohistochemically the expression of the main markers like somatostatin (SOM), parvalbumin (PV), calretinin (CR), calbindin (CB), neuropeptide Y (NPY) and/or nitric oxide synthase (NOS) at the pallial regions of three different models of Osteichthyes. First, we selected two tetrapods, one amniote from the genus Pseudemys belonging to the order Testudine, at the base of the amniote diversification and with a three-layered simple cortex, and the Anuran Xenopus laevis, an anamniote tetrapod with a non-layered evaginated pallium, and finally the order Polypteriform, a small fish group at the base of the actinopterygian diversification with an everted telencephalon. SOM was the most conserved interneuron type in terms of its distribution and co-expression with other markers such as CR, in contrast to PV, which showed a different pattern between the models analyzed. In addition, the SOM expression supports a homological relationship between the medial pallial derivatives in all the models. CR and CB expressions in the tetrapods were observed, particularly, CR expressing cells were detected in the medial and the dorsal pallial derivatives, in contrast to CB, which appeared only in discrete scattered populations. However, the pallium of Polypteriforms fishes was almost devoid of CR cells, in contrast to the important number of CB cells observed in all the pallial regions. The NPY immunoreactivity was detected in all the pallial domains of all the models, as well as cells coexpressing CR. Finally, the pallial nitrergic expression was also conserved, which allows to postulate the homological relationships between the ventropallial and the amygdaloid derivatives. In summary, even in basal pallial models the neurochemically characterized interneurons indicate that their first appearance took place before the common ancestor of amniotes. Thus, our results suggest a shared pattern of interneuron types in the pallium of all Osteichthyes.
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Abbreviations
- Amy:
-
Amygdaloid complex
- BG:
-
Basal ganglia
- BST:
-
Bed nucleus of the stria terminalis
- CB:
-
Calbindin
- CeA:
-
Central amygdala
- CR:
-
Calretinin
- DCx:
-
Dorsal cortex
- DP:
-
Dorsal pallium
- DVR:
-
Dorsal ventricular ridge
- Hb:
-
Habenulae
- LA:
-
Latereal amygdala
- LCx:
-
Lateral cortex
- LP:
-
Lateral pallium
- MCx:
-
Medial cortex
- MeA:
-
Medial amygdala
- MP:
-
Medial pallium
- NOS:
-
Nitric oxide synthase
- NPY:
-
Neuropeptide Y
- P1, P2, P3:
-
Pallial fields of polypteriform fishes
- P1d:
-
Dorsal part of pallial field P1
- P1v:
-
Ventral part of pallial field P1
- PT:
-
Pallial thickening
- PV:
-
Parvalbumin
- S:
-
Septum
- Str:
-
Striatum
- SOM:
-
Somatostatin
- SPa:
-
Subpallium
- Th:
-
Thalamus
- v:
-
Ventricle
- VP:
-
Ventral pallium
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This work was supported by a Spanish MICINN grant, Grant/award number: BFU2015-66041P and Universidad Complutense de Madrid, Grant/Award Number: PR87/19-22546.
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All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. NM devised the study. SJ, RM and NM performed the experiments with Xenopus and Pseudemys. DL and JML performed the experiments with polypteriform fishes. NM and SJ analyzed the results, led the figure preparation and wrote the article, corrected and edited by JML and AG. All authors approved the article.
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The authors declare no conflicts of interest. The original research reported herein was performed according to the regulations and laws established by European Union (2010/63/EU) and Spain (Royal Decree 1386/2018) for care and handling of animals in research and after approval from the Complutense University to conduct the experiments described.
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429_2020_2123_MOESM2_ESM.tif
Supplementary file2 Supplementary Fig. 1. Photomicrographs of transverse sections through the telencephalon of Pseudemys scripta (a–d), Xenopus laevis (e-k) and Polypterus senegalus (l-r), at rostral (a, l, m), medial (b, e–l, n, o) and caudal (c, d, j, k) levels showing Tbr1 (a–c, e, l, n) and Tbr1/Isl1 (d, f–k, m, o) expressions. The color codes are indicated in each photo. Scale bar in a–g, j, l, n=100 µm; h, i, k, m, o =500 µm. See abbreviation list (TIF 33593 kb)
429_2020_2123_MOESM3_ESM.tif
Supplementary file3 Supplementary Fig. 2. Photomicrographs of transverse sections through the telencephalon of Pseudemys scripta (a–e), Xenopus laevis (f–h) and Polypterus senegalus (i–k), showing, from rostral to caudal levels, GABA expression. Arrowheads point to immunoreactive cell bodies in the pallium. Scale bar in a, c, f-h, j, k=200 µm; b, i =500 µm; d, e = 100 µm. See abbreviation list (TIF 37880 kb)
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Jiménez, S., López, J.M., Lozano, D. et al. Analysis of pallial/cortical interneurons in key vertebrate models of Testudines, Anurans and Polypteriform fishes. Brain Struct Funct 225, 2239–2269 (2020). https://doi.org/10.1007/s00429-020-02123-5
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DOI: https://doi.org/10.1007/s00429-020-02123-5