Dynamic expression of tyrosine hydroxylase mRNA and protein in neurons of the striatum and amygdala of mice, and experimental evidence of their multiple embryonic origin

Abstract

Emotional and motivational dysfunctions observed in Parkinson’s disease, schizophrenia, and drug addiction are associated to an alteration of the mesocortical and mesolimbic dopaminergic pathways, which include axons projecting to the prefrontal cortex, the ventral striatum, and the amygdala. Subpopulations of catecholaminergic neurons have been described in the cortex and striatum of several mammals, but the presence of such cells in the adult amygdala is unclear in murine rodents, and in other rodents appears to show variations depending on the species. Moreover, the embryonic origin of telencephalic tyrosine hydroxylase (TH) cells is unknown, which is essential for trying to understand aspects of their evolution, distribution and function. Herein we investigated the expression of TH mRNA and protein in cells of the striatum and amygdala of developing and adult mice, and analyzed the embryonic origin of such cells using in vitro migration assays. Our results showed the presence of TH mRNA and protein expressing cells in the striatum (including nucleus accumbens), central and medial extended amygdala during development, which are persistent in adulthood although they are less numerous, generally show weak mRNA expression, and some appear to lack the protein. Fate mapping analysis showed that these cells include at least two subpopulations with different embryonic origin in either the commissural preoptic area of the subpallium or the supraopto-paraventricular domain of the alar hypothalamus. These data are important for future studies trying to understand the role of catecholamines in modulation of emotion, motivation, and reward.

Embryonic Origin of the Islet1 and Pax6 Neurons of the Chicken Central Extended Amygdala Using Cell Migration Assays and Relation to Different Neuropeptide-Containing Cells

“…More recently, the embryonic commissural PO was also shown to produce a minor subpopulation of catecholaminergic neurons for the EAce and St in mice [Bupesh et al, 2014], and a similar contribution was also suggested to occur in chicken ( fig. 10 ) .…”

“…10 b), but it is unknown whether they represent the same or different subtypes. In the mouse, the LGEd/Std produce catecholaminergic cells for the olfactory bulb and Tu [Yun et al, 2003], and this is likely similar in other vertebrates [discussed by Abellán and Medina, 2009], but it is unclear whether the mouse LGEd also produces catecholaminergic cells for the ITC [Bupesh et al, 2014] fig. 10 b).…”

“…However, based on the available data (e.g. Moreno et al [2012b] for the BST), the EAce of amphibians does not appear to include the Std-derived and PO-derived cells [Moreno et al, 2008a;Domínguez et al, 2010;Moreno et al, 2012b], although the caudal parts of the BST include a few catecholaminergic neurons [Moreno et al, 2012b] that resemble those found in the EAce of the mouse and chicken with putative preoptic origin [Bupesh et al, 2014;Vicario et al, 2014]. Based on the combination of transcription factors involved in the development of either GABAergic (Dlx and Mash1) or glutamatergic (Tbr1, NeuroD and Neurogenin 2) cells, together with the expression of GABAergic markers (including the enzyme glutamic acid decarboxylase) [Osorio et al, 2010], the subpallial-derived neurons of the amphibian EAce (which make up the majority of the EAce cells, as in other tetrapods) are GABAergic, while those coming from the EMT or the pallium are glutamatergic [Brox et al, 2003[Brox et al, , 2004Wullimann et al, 2005;Moreno et al, 2012b].…”

Evolutionary and Developmental Contributions for Understanding the Organization of the Basal Ganglia

“…For abbreviations see list. Abellán, 2012;Bupesh et al, 2013]. Regarding tangential migrations, the first to be described were those from the MGE and the adjacent entopeduncular area 2 to the caudoputamen; they were demonstrated to produce most subtypes of striatal interneurons, including those containing parvalbumin (PV), those containing acetylcholine, most of the neuropeptide Y/somatostatin/nitric oxide synthase-expressing interneurons, and most of the calretinin-containing interneurons [Marín et al, 2000].…”

“…Recent evidence has shown that most (if not all) cholinergic interneurons of the caudoputamen really originate in the preoptic area and depend on the expression of both Lhx7/8 and Islet1 [Elshatory and Gan, 2008;García-López et al, 2008; reviewed by Medina and Abellán, 2012]. In addition, a recent study showed that most of the dopaminergic interneurons of the striatum also migrate tangentially from the preoptic area [Bupesh et al, 2013]. In contrast to most interneurons, projection neurons of the caudoputamen (containing either substance P, SP, or enkephalin, ENK, amounting to 90-95% of all striatal neurons [Medina and Reiner, 1995]) originate in the LGE and migrate radially into the mantle [Marín and Rubenstein, 2001].…”