Top

Published in:

Open Access 01-09-2020 | Original Article

A radial histogenetic model of the mouse pallial amygdala

Authors: Elena Garcia-Calero, Margaret Martínez-de-la-Torre, Luis Puelles

Published in: Brain Structure and Function | Issue 7/2020

Abstract

Conventional anatomic models of the rodent (mammalian) amygdala are based on section planes oblique to its intrinsic radial glial organization. As a result, we still lack a model of amygdalar histogenesis in terms of radial units (progenitor domains and related radial migration and layering patterns). A radial model of the mouse pallial amygdala is first offered here, based on three logical steps: (1) analysis of amygdalar radial structure in variously discriminative genoarchitectonic material, using an optimal ad hoc section plane; (2) testing preliminary models with experiments labelling at the brain surface single packets of radial glia processes, to be followed into the ventricular surface across intervening predicted elements; (3) selection of 81 differential amygdalar gene markers and checking planar and radial aspects of their distribution across the model elements. This approach shows that subtle changes to the conventional schema of the amygdala allow a radial histogenetic model to be recognized, which is consistent with molecularly coded differential identities of its units and strata. It is expected that this model will help both causal studies of amygdalar developmental patterning and comparative evolutionary studies. It also may have potential impact on hodological and functional studies.

Available only for authorised users

Abellán A, Desfilis E, Medina L (2014) Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. Front Neuroanat 8:59. https://doi.org/10.3389/fnana.2014.00059CrossRefPubMedPubMedCentral

Abellán A, Legaz I, Vernier B, Rétaux S, Medina L (2009) Olfactory and amygdalar structures of the chicken ventral pallium based on the combinatorial expression patterns of LIM and other developmental regulatory genes. J Comp Neurol 516:166–186. https://doi.org/10.1002/cne.22102CrossRefPubMed

Alheid GF, de Olmos J, Beltramino CA (1995) Amygdala and extended amygdala. In: Paxinos G (ed) The Rat Nervous System. Academic Press, San Diego, pp 495–578

Bayer SA (1980) Quantitative 3H-thymidine radiographic analyses of neurogenesis in the rat amygdala. J Comp Neurol 194:845–875PubMed

Berdel B, Moryś J (2000) Expression of calbindinD28k and parvalbumin during development of rat's basolateral amygdaloid complex. Int J Dev Neurosci 18:501–513

Brockhaus H (1938) Zur normalen und pathologischen Anatomie des Mandelkerngebietes (Subzona semicorticalis amygdalae und Subzona claustralis praeamygdalea). J Psychol Neurol 49:1–136

Cassell MD, Gray TS, Kiss JZ (1986) Neuronal architecture in the rat central nucleus of the amygdala: a cytological, hodological, and immunocytochemical study. J Comp Neurol 246:478–499PubMed

Cocas LA, Georgala PA, Mangin JM, Clegg JM, Kessaris N, Haydar TF, Gallo V, Price DJ, Corbin JG (2011) Pax6 is required at the telencephalic pallial-subpallial boundary for the generation of neuronal diversity in the postnatal limbic system. J Neurosci 31:5313–5324. https://doi.org/10.1523/JNEUROSCI.3867-10CrossRefPubMedPubMedCentral

De Olmos JS, Beltramino CA, Alheid G (2004) Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In: Paxinos G (ed) The Rat Nervous System, 3rd edn. Elsevier-Academic Press, Amsterdam, pp 509–603

Ferran JL, Puelles L, Rubenstein JL (2015) Molecular codes defining rostrocaudal domains in the embryonic mouse hypothalamus. Front Neuroanat 9:46. https://doi.org/10.3389/fnana.2015.00046CrossRefPubMedPubMedCentral

Garcia-Calero E, Scharff C (2013) Calbindin expression in developing striatum of zebra finches and its relation to the formation of area X. J Comp Neurol 521:326–341. https://doi.org/10.1002/cne.23174CrossRefPubMed

García-López M, Abellán A, Legaz I, Rubenstein JL, Puelles L, Medina L (2008) Histogenetic compartments of the mouse centromedial and extended amygdala based on gene expression patterns during development. J Comp Neurol 506:46–74PubMedPubMedCentral

Gastaut H, Lammers HJ (1961) Anatomie du Rhinencéphale. Les Grandes Activités du Rhinencéphale Vol.1 (Alajouanine Th, ed), Masson & Cie., Paris.

Gloor P (1997) The temporal lobe and limbic system. Oxford Univ. Press, New York and Oxford

Hirata T, Li P, Lanuza GM, Cocas LA, Huntsman MM, Corbin JG (2009) Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala. Nat Neurosci 12:141–149. https://doi.org/10.1038/nn.2241CrossRefPubMedPubMedCentral

Holmgren N (1925) Points of view concerning forebrain morphology in higher vertebrates. Acta Zool 6:413–477

Jacobowitz DM, Abbott LC (1997) Chemoarchitectonic atlas of the developing mouse brain. CRC Press, Boca Raton

Johnston JB (1923) Further contributions to the study of the evolution of the forebrain. J Comp Neurol 35:337–481

Kemppainen S, Pitkänen A (2000) Distribution of parvalbumin, calretinin, and calbindin-D(28k) immunoreactivity in the rat amygdaloid complex and colocalization with gammaaminobutyric acid. J Comp Neurol 426:441–467PubMed

Krettek JE, Price JL (1978) A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol 178:255–280PubMed

Lammers GJ (1976) On the development of the strio-amygdaloid complex in the Chinese hamster, Cricetulus griseus. Krips Repro Meppel (Ed), The Netherlands.

LeDoux J (2007) The amygdala. Curr Biol 17:R868–874PubMed

Legaz I, Olmos L, Real MA, Guirado S, Dávila JC, Medina L (2005) Development of neurons and fibers containing calcium binding proteins in the pallial amygdala of mouse, with special emphasis on those of the basolateral amygdalar complex. J Comp Neurol 488:492–513PubMed

López-Garcia C1, Ramos-Molina B, Lambertos A, López-Contreras AJ, Cremades A, Peñafiel R (2013) Antizyme inhibitor 2 hypomorphic mice. New patterns of expression in pancreas and adrenal glands suggest a role in secretory processes. PLoS One 8:e69188. https://doi.org/10.1371/journal.pone.0069188

Martínez-García F, Noverjarque A, Guitiérrez-Castellanos N, Lanuza E (2012) Piriform cortex and amygdala. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic Press, San Diego, CA, pp 140–172

Martínez-García F, Novejarque A, Lanuza E (2008) Two interconnected functional systems in the amygdala of amniote vertebrates. Brain Res Bull 75:206–213. https://doi.org/10.1016/j.brainresbull.2007.10.019CrossRefPubMed

Martinez-de-la-Torre M, Lambertos A, Peñafiel R, Puelles L (2018) An exercise in brain genoarchitectonics: analysis of AZIN2-Lacz expressing neuronal populations in the mouse hindbrain. J Neurosci Res 96:1490–1517. https://doi.org/10.1002/jnr.24053CrossRefPubMed

McDonald AJ (2003) Is there an amygdala and how far does it extend? An anatomical perspective. Ann NY Acad Sci 985:1–21PubMed

McDonald AJ, Augustine JR (1993) Localization of GABA-like immunoreactivity in the monkey amygdala. Neuroscience 52:281–294PubMed

Medina L, Abellán A, Vicario A, Castro-Robles B, Desfilis E (2017) The Amygdala. In: Kaas J (ed) Evolution of Nervous Systems 2e, vol 1. Elsevier, Oxford, pp 427–478

Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–741PubMed

Medina L, Legaz I, González G, de Castro F, Rubenstein JLR, Puelles L (2004) Expression of Dbx1, neurogenin 2, semaphorin 5A, cadherin 8, and emx1 distinguish ventraland lateral pallial histogenetic divisions in the developing claustroamygdaloid complex. J Comp Neurol 474:504–523PubMed

Nery S, Fishell G, Corbin JG (2002) The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279–1287PubMed

Nieuwenhuys R, Nicholson C (1998) Lampreys (Petromyzontoidea). In: Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrates, vol 1. Springer, Berlin, pp 397–495

Nieuwenhuys R, Puelles L (2016) Towards a new neuromorphology. Springer International Publishing, Switzerland

Olucha-Bordonau FE, Fortes-Marco L, Otero-García M, Lanuza E, Martínez-García F (2015) Amygdala: structure and function. The Rat Nervous System. Academic Press, San Diego, CA, pp 442–476

Paxinos G, Ashwell KWS, Tork I (1994) Atlas of the developing rat nervous system. Academic Press, San Diego, CA

Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego, CA

Paxinos G, Franklin KBJ (2013) The mouse brain in stereotaxic coordinates. Academic Press, San Diego, CA

Paxinos G, Watson C (2014) The rat brain in stereotaxic coordinates, 7th edn. Academic Press/Elsevier, Amsterdam

Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187PubMed

Price JL, Russchen FT, Amaral DG (1987) The limbic system. II. The amygdaloid complex. Handbook of Chemical Neuroanatomy. In: Björklund A, Hökfelt T, Swanson LW (eds) Integrated systems of the CNS, Part I: Hypothalamus, Hippocampus, Amygdala, Retina, vol 5. Elsevier, Amsterdam, New York, Oxford, pp 279–388.

Puelles L (2014) Development and evolution of the claustrum. Elsevier, The Claustrum

Puelles L, Alonso A, García-Calero E, Martínez-de-la-Torre M (2019) Concentric ring topology of mammalian cortical sectors and relevance for patterning studies. J Comp Neurol 527:1731–1752. https://doi.org/10.1002/cne.24650CrossRefPubMed

Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JLR (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438PubMed

Puelles L, Medina L (2002) Field homology as a way to reconcile genetic and developmental variability with adult homology. Brain Res Bull 57:243–255PubMed

Puelles L, Medina L, Borello U, Legaz I, Teissier A, Pierani A, Rubenstein JLR (2016a) Radial derivatives of the mouse ventral pallium traced with Dbx1-LacZ reporters. J Chem Neuroanat 75:2–19. https://doi.org/10.1016/j.jchemneu.2015.10.011CrossRefPubMed

Puelles L, Morales-Delgado N, Merchán P, Castro-Robles B, Martínez-de-la-Torre M, Díaz C, Ferran JL (2016b) Radial and tangential migration of telencephalic somatostatin neurons originated from the mouse diagonal area. Brain Struct Funct 221:3027–3065. https://doi.org/10.1007/s00429-015-1086-8CrossRefPubMed

Remedios R, Subramanian L, Tole S (2004) LIM genes parcellate the embryonic amygdala and regulate its development. J Neurosci 24:6986–6990PubMedPubMedCentral

Remedios R, Huilgol D, Saha B, Hari P, Bhatnagar L, Kowalczyk T, Hevner RF, Suda Y, Aizawa S, Ohshima T, Stoykova A, Tole S (2007) A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex. Nat Neurosci 10:1141–1150PubMed

Rolls ET (2015) Limbic systems for emotion and for memory, but no single limbic system. Cortex 62:119–157. https://doi.org/10.1016/j.cortex.2013.12.005CrossRefPubMed

Ruiz-Reig N, Andres B, Lamonerie T, Theil T, Fairén A, Studer M (2018) The caudo-ventral pallium is a novel pallial domain expressing Gdf10 and generating Ebf3-positive neurons of the medial amygdala. Brain Struct Funct 223:3279–3295. https://doi.org/10.1007/s00429-018-1687-0CrossRefPubMed

Sah P, Faber ES, De Armentia L, Power J (2003) The amygdalar complex: anatomy and physiology. Physiol Rev 83:803–834

Shimamura K, Hirano S, McMahon AP, Takeichi M (1994) Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development 120:2225–2234PubMed

Silberberg SN, Taher L, Lindtner S, Sandberg M, Nord AS, Vogt D, Mckinsey GL, Hoch R, Pattabiraman K, Zhang D, Ferran JL, Rajkovic A, Golonzhka O, Kim C, Zeng H, Puelles L, Visel A, Rubenstein JLR (2016) Subpallial enhancer transgenic lines: a data and tool resource to study transcriptional regulation of GABAergic cell fate. Neuron 92:59–74. https://doi.org/10.1016/j.neuron.2016.09.027CrossRefPubMedPubMedCentral

Stenman J, Yu RT, Evans RM, Campbell K (2003) Tlx and Pax6 co-operate genetically to establish the pallio-subpallial boundary in the embryonic mouse telencephalon. Development 130:1113–1122PubMed

Striedter G, Northcutt RG (2020) Brains through Time. New York, Oxford University Press, A Natural History of Vertebrates

Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331PubMed

Sun N, Cassell MD (1993) Intrinsic GABAergic neurons in the rat central extended amygdala. J Comp Neurol 330:381–404PubMed

Tang K, Rubenstein JL, Tsai SY, Tsai MJ (2012) COUP-TFII controls amygdala patterning by regulating neuropilin expression. Development 139:1630–1639. https://doi.org/10.1242/dev.075564CrossRefPubMedPubMedCentral

Tole S, Remedios R, Saha B, Stoykova A (2005) Selective requirement of Pax6, but not Emx2, in the specification and development of several nuclei of the amygdaloid complex. J Neurosci 25:2753–2760PubMedPubMedCentral

Tosches MA, Yamawaki TM, Naumann RK, Jacobi AA, Tushev G, Laurent G (2018) Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360:881–888. https://doi.org/10.1126/science.aar4237CrossRefPubMed

Turner BH, Zimmer J (1984) The architecture and some of the interconnections of the rat's amygdala and lateral periallocortex. J Comp Neurol 227:540–557PubMed

Whalen PJ, Phelps EA (2009) The human amygdala. The Guilford Press, New York

Wicht H, Nieuwenhuys R (1998) Hagfishes (Myxinoidea). In: Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrates, vol 1. Springer, Berlin, pp 497–549

Voigt T (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74–88PubMed

Title: A radial histogenetic model of the mouse pallial amygdala
Authors: Elena Garcia-Calero
Margaret Martínez-de-la-Torre
Luis Puelles
Publication date: 01-09-2020
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 7/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-020-02097-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

A radial histogenetic model of the mouse pallial amygdala

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2020

Functional and structural correlates of the preterm infant’s brain: relating developmental changes of auditory evoked responses to structural maturation

Postnatal exposure to an acoustically enriched environment alters the morphology of neurons in the adult rat auditory system

Male-specific features are reduced in Mecp2-null mice: analyses of vasopressinergic innervation, pheromone production and social behaviour

Correction to: Effects of transcranial direct current stimulation of left and right inferior frontal gyrus on creative divergent thinking are moderated by changes in inhibition control

Involvement of the lateral habenula in fear memory

Thyrotropin-releasing hormone axonal varicosities appear to innervate dopaminergic neurons in the human hypothalamus