Differences in Neurogenesis Differentiate between Core and Shell Regions of Auditory Nuclei in the Turtle <i>(Pelodiscus sinensis):</i> Evolutionary Implications

Abstract

There is a clear core-versus-shell distinction in cytoarchitecture, electrophysiological properties and neural connections in the mesencephalic and diencephalic auditory nuclei of amniotes. Determining whether the embryogenesis of auditory nuclei shows a similar organization is helpful for further understanding the constituent organization and evolution of auditory nuclei. Therefore in the present study, we injected [³H]-thymidine into turtle embryos (Pelodiscus sinensis) at various stages of development. Upon hatching, [³H]-thymidine labeling was examined in both the core and shell auditory regions in the midbrain, diencephalon and dorsal ventricular ridge. Met-enkephalin and substance P immunohistochemistry was used to distinguish the core and shell regions. In the mesencephalic auditory nucleus, the occurrence of heavily labeled neurons in the nucleus centralis of the torus semicircularis reached its peak at embryonic day 9, one day later than the surrounding shell. In the diencephalic auditory nucleus, the production of heavily labeled neurons in the central region of the reuniens (Re) was highest at embryonic day (E) 8, one day later than that in the shell region of reuniens. In the region of the dorsal ventricular ridge that received inputs from the central region of Re, the appearance of heavily labeled neurons also reached a peak one day later than that in the area receiving inputs from the shell region of reuniens. Thus, there is a core-versus-shell organization of neuronal generation in reptilian auditory areas.

Evolutionary significance of delayed neurogenesis in the core versus shell auditory areas of Mus musculus

“…Consistent with its physiological functions and broad neural connections, the shell regions have rich distributions of various neurotransmitters and other neuroactive substances, including serotonin (5‐HT), enkephalin (ENK), substance P (SP), calcitonin gene‐related peptide calbindin (CGRP), and calbindin (CB). However, these chemicals are either absent from, or not dominantly located in, the core regions (reptiles: Brauth and Reiner,1991; Belekhova et al,2002; Zeng et al,2007b; birds: Martinez‐Vargas et al,1976; Reubi and Jessell,1978; Blähser and Dubois,1980; De Lanerolle et al,1981; Erichsen et al,1991; Durand et al,1992; Puelles et al,1994; mammals: Cuello and Kanazwa,1978; Fallon and Leslie,1986; Nakagawa et al,1995; Peruzzi and Dut,2004). This core‐to‐shell distinction, however, is only obvious in mesencephalic, but not diencephalic, auditory areas of amphibians, and fish lack this difference in both regions (amphibians: Feng and Lin,1991; Simmons et al,2000; Edwards and Kelley2001; Zeng et al,2007a,2008a; fish: Echteler,1985a,b; Cuadrado,1987; Schellart et al,1987; Crespo et al,1999; Clemente et al,2005).…”

“…Recently, we found an additional occurrence of this core‐to‐shell dissimilarity that was associated with neurogenesis. The onset of neuronal generation was generally delayed in the core compared to the shell regions (Zeng et al,2007b,2008a,b). This distinction was observed in the mesencephalic to the telencephalic auditory areas of reptile and bird, but it was seen only in the mesencephalic auditory area of amphibian.…”

Distinction in the immunoreactivities of two calcium‐binding proteins and neuronal birthdates in the first and higher‐order somatosensory thalamic nuclei of mice: Evolutionary implications

“…To visualize the tissue cytoarchitectures and cellular morphologies, the sections were counterstained with cresyl violet. The detailed autoradiographic procedures have been previously described (Zeng et al, ).…”

“…Additionally, the generation of cells in the core auditory regions of amniotes is significantly delayed in the ventricle zone relative to the cells in the diffuse regions (Zeng et al, , ,b, ), and positive CB staining occurs earlier than PV immunoreactivity during embryonic development (Xi et al, ). In light of the concept of Von Baerian recapitulation, early animal embryos within a taxon resemble each other, and the degree of resemblance decreases as development proceeds (Gould, ; Butler, ; Northcutt, ).…”

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

“…In this study, we follow the subdivisions and some of the nomenclature introduced by Puelles et al (1994) and Robles-Moreno (1995). We focus only on the auditory central nucleus of the torus or toral nucleus, separate from the surrounding areas, which are sometimes referred to as the shell (Zeng et al, 2007;Browner and Baruch, 1984;Browner and Rubinson, 1977). The central nucleus is the recipient of the lateral lemniscal fibers (Foster and Hall, 1978) and projects to the auditory nucleus of the thalamus (Foster and Hall, 1978;Kennedy and Browner, 1981;Pritz, 1974;ten Donkelaar et al, 1987).…”