New perspective on the regionalization of the anterior forebrain in Osteichthyes

Abstract

In the current model, the most anterior part of the forebrain (secondary prosencephalon) is subdivided into the telencephalon dorsally and the hypothalamus ventrally. Our recent study identified a new morphogenetic unit named the optic recess region (ORR) between the telencephalon and the hypothalamus. This modification of the forebrain regionalization based on the ventricular organization resolved some previously unexplained inconsistency about regional identification in different vertebrate groups. The ventricular-based comparison also revealed a large diversity within the subregions (notably in the hypothalamus and telencephalon) among different vertebrate groups. In tetrapods there is only one hypothalamic recess, while in teleosts there are two recesses. Most notably, the mammalian and teleost hypothalami are two extreme cases: the former has lost the cerebrospinal fluid-contacting (CSF-c) neurons, while the latter has increased them. Thus, one to one homology of hypothalamic subregions in mammals and teleosts requires careful verification. In the telencephalon, different developmental processes between Sarcopterygii (lobe-finned fish) and Actinopterygii (ray-finned fish) have already been described: the evagination and the eversion. Although pallial homology has been long discussed based on the assumption that the medial-lateral organization of the pallium in Actinopterygii is inverted from that in Sarcopterygii, recent developmental data contradict this assumption. Current models of the brain organization are largely based on a mammalian-centric point of view, but our comparative analyses shed new light on the brain organization of Osteichthyes.

Organization of the catecholaminergic systems in the brain of lungfishes, the closest living relatives of terrestrial vertebrates

“…This situation seems to be shared by all vertebrates with the only exception of placental mammals, which have lost the TH2 gene and lack CSF‐contacting cells in the hypothalamus (Yamamoto & Vernier, ). Our data in lungfishes suggest that both DA and 5‐HT might be co‐expressed in NPv cells, in agreement with recent data in teleosts, amphibians, and birds, in which it was demonstrated that many CSF‐contacting cells coexpress TH2 and tryptophan hydroxylase 1 (TPH1) and contain both DA and 5‐HT, reinforcing the idea that this characteristic is inherited from the common ancestor of the Osteichthyes (Xavier et al, ; Yamamoto et al, ).…”

“…Suprachiasmatic cells labeled with the DA antibody but not with the TH antibody in Protopterus suggest that these cells synthesize catecholamines through TH2, the enzyme that is not detected with the used antibodies (Yamamoto et al, ). It should be noted that when this situation has been observed in other vertebrate groups, the DA positive cells were CSF‐contacting cells (Xavier et al, ; Yamamoto, Bloch, & Vernier, ), different from the observation in lungfishes. In addition, we observed TH positive but DA negative cells in the suprachiasmatic nucleus.…”

“…Like in teleosts, amphibians and birds, these cells are not labeled with the generally used antibodies that detect TH1 (Smeets & González, ; Yamamoto et al, ; Xavier et al, ). A possibility was raised that these cells accumulate extracellular DA by a mechanism of uptake from the ventricular CSF rather than synthesizing it (Smeets & González, ; Smeets & Steinbusch, ), but recent data strongly support that the NPv cells are actual DA‐synthesizing cells that use TH2 as first enzyme instead of TH1 (Yamamoto et al, ; Xavier et al, ). This situation seems to be shared by all vertebrates with the only exception of placental mammals, which have lost the TH2 gene and lack CSF‐contacting cells in the hypothalamus (Yamamoto & Vernier, ).…”

Organization of the Orexin/Hypocretin System in the Brain of Holostean Fishes: Assessment of Possible Relationships with Monoamines and Neuropeptide Y

“…These ar-Brain Behav Evol 2018;91:228-251 DOI: 10.1159/000490172 eas were proposed to correspond to the medial and dorsal pallial regions, respectively, of the noneverted telencephalon of tetrapods [Yamamoto et al, , 2017. This limited distribution of OX-ir fibers in pallial/cortical regions is a general feature described in all groups of vertebrates studied (Table 2).…”

Preface to Vertebrate Brains: evolution, structures and functions

“…Yamamoto et al . () review regionalization of the anterior part of the forebrain of Osteichtyes (bony fish). The anterior part of the forebrain is subdivided into the telencephalon dorsally and the hypothalamus ventrally.…”