Abstract

We focus this report on the nucleus of the lateral olfactory tract (NLOT), a superficial amygdalar nucleus receiving olfactory input. Mixed with its Tbr1-expressing layer 2 pyramidal cell population (NLOT2), there are Sim1-expressing cells whose embryonic origin and mode of arrival remain unclear. We examined this population with Sim1-ISH and a Sim1-tauLacZ mouse line. An alar hypothalamic origin is apparent at the paraventricular area, which expresses Sim1 precociously. This progenitor area shows at E10.5 a Sim1-expressing dorsal prolongation that crosses the telencephalic stalk and follows the terminal sulcus, reaching the caudomedial end of the pallial amygdala. We conceive this Sim1-expressing hypothalamo-amygdalar corridor (HyA) as an evaginated part of the hypothalamic paraventricular area, which participates in the production of Sim1-expressing cells. From E13.5 onwards, Sim1-expressing cells migrated via the HyA penetrate the posterior pallial amygdalar radial unit and associate therein to the incipient Tbr1-expressing migration stream which swings medially past the amygdalar anterior basolateral nucleus (E15.5), crosses the pallio-subpallial boundary (E16.5), and forms the NLOT2 within the anterior amygdala by E17.5. We conclude that the Tbr1-expressing NLOT2 cells arise strictly within the posterior pallial amygdalar unit, involving a variety of required gene functions we discuss. Our results are consistent with the experimental data on NLOT2 origin reported by Remedios et al. (Nat Neurosci 10:1141–1150, 2007), but we disagree on their implication in this process of the dorsal pallium, observed to be distant from the amygdala.

Highlights

  • The mammalian amygdalar pallial complex consists of a heterogeneous group of nuclei located in the telencephalic temporal pole, rostrally to the caudo ventral hippocampus

  • In the second phase of this study, we related the amygdalar population of Sim1-expressing cells to the rostrally migrating stream of Tbr1-expressing pallial cells which constitute what we call the NLOT2 migratory stream (NLOT2ms), known as caudal amygdalar stream, or caudal amygdalar migratory stream (CAS). We found that this pallial stream starts at the posterior pallial amygdalar unit we recently defined (Garcia-Calero et al 2020), which is the anlage of the amygdalo-hippocampal area and the posteromedial cortical nucleus (AHi/PMCo complex)

  • We subsequently compared immunocytochemically Sim1 signal with the expression of Otp and Tbr1 proteins, and with the radial glia marker RC2, applying the recently proposed amygdalar radial section plane (Garcia-Calero et al 2020). This plane is oblique to the conventional coronal plane, and forms a varying angle of 30°–45° with reference to a line tangent to the entorhinal cortex at the back of the hemisphere; this plane agrees with the spatial disposition of radial glial processes crossing the amygdalar pallial region (Fig. 4h–m)

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Summary

Introduction

The mammalian amygdalar pallial complex consists of a heterogeneous group of nuclei located in the telencephalic temporal pole, rostrally to the caudo ventral hippocampus. Garcia-Calero et al (2020) described in addition a cell-sparse NLOT shell formation of genoarchitecturally distinct neurons (Azin2-, Er81, and Cyp26-positive) contributing likewise to layer 3. This shell is continuous with a tail of similar neurons leading backwards along the former migration trail of the NLOT2 up to the medial horn of the basolateral nucleus (BLA). We named the new entity the ‘amygdalo-olfactory stream’ (Garcia-Calero et al 2020)

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