Trends in Neurosciences
Volume 36, Issue 10, October 2013, Pages 570-578
Journal home page for Trends in Neurosciences

Opinion
A developmental ontology for the mammalian brain based on the prosomeric model

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Highlights

  • We have used the prosomeric model to create a modern ontology of mammalian brain structures.

  • This ontology is based chiefly on gene expression during development.

  • This ontology will be useful to the field of neuroinformatics.

In the past, attempts to create a hierarchical classification of brain structures (an ontology) have been limited by the lack of adequate data on developmental processes. Recent studies on gene expression during brain development have demonstrated the true morphologic interrelations of different parts of the brain. A developmental ontology takes into account the progressive rostrocaudal and dorsoventral differentiation of the neural tube, and the radial migration of derivatives from progenitor areas, using fate mapping and other experimental techniques. In this review, we used the prosomeric model of brain development to build a hierarchical classification of brain structures based chiefly on gene expression. Because genomic control of neural morphogenesis is remarkably conservative, this ontology should prove essentially valid for all vertebrates, aiding terminological unification.

Section snippets

What is ontology?

The concept of ontology (see Glossary) was borrowed from the realm of philosophy by information scientists, who now use it as a way to represent an existing domain of knowledge in the form of a hierarchical taxonomy [1]. The availability of a brain ontology is vital for the field of neuroinformatics. There have been several attempts to create a brain ontology, the most notable of which are NeuroNames 2, 3, 4, the Biomedical Information Research Network (BIRN) [5], and the Brain Architecture

Comparing traditional and developmental ontologies

All adult brain ontologies start with the recognition of three basic elements: forebrain, midbrain, and hindbrain. Even at this level, the developmental ontology is distinctive, in that it includes the isthmus within the hindbrain, rather than in the midbrain, as found in traditional ontologies. The importance of transgenic fate mapping to the understanding of such delimitation has been emphasized previously 10, 11, 12.

There are many novel features at the next hierarchical level of the

Herrick and the ‘columnar’ forebrain axis

Twentieth-century ideas on forebrain subdivisions were dominated by the columnar model of the forebrain put forward by Herrick [42]. Contradicting the earlier analysis of His [43], Herrick proposed that the brainstem axis simply extended rostrally as a straight line into the forebrain, so that the thalamus–hypothalamus complex (then called the diencephalon) stood in direct axial continuity with the telencephalon rostrally and the midbrain caudally. This concept was not based on developmental

Neuromeres

Periodic transverse outpouchings in the neural tube wall were first recognized over a century ago (12, 50, 51). Orr [51] called them neuromeres (prosomeres in the prosencephalon, mesomeres in the midbrain, and rhombomeres in the hindbrain), thus viewing them as neural segments within the general plan of head segmentation (Figure 1D). The neuromere concept fell into disuse with the rise in popularity of Herrick's columnar paradigm, basically because brain segments did not offer at that time a

Pallium and subpallium

The telencephalic hemisphere is not an axial vesicle, because there are two of them. It is formed by an idiosyncratic patterning mechanism that generates pallial and subpallial regions that are already at neural plate stages 88, 89, 90, 91. The traditional columnar misconception that the longitudinal axis of the brain ends in the telencephalon has resulted in the widespread assumption that the embryonic pallium lies dorsal to the embryonic subpallium; in reality, the pallium is topologically

Concluding remarks

A new brain ontology based on modern developmental criteria and models provides a more accurate and complete view of the natural morphologic interrelations of different parts of the brain. Neuronal populations have been classified on the basis of progressive rostrocaudal and dorsoventral differentiation of the neural tube. Radially migrated (stratified) derivatives can be traced from progenitor areas based on fate mapping, gene mapping, and other experimental evidence. Overall, this

Glossary

Diencephalon
the caudal subdivision of the forebrain that joins the midbrain to the secondary prosencephalon; it contains three major alar domains (pretectum, thalamus, and prethalamus), as well as the corresponding tegmental regions.
Evo-devo
an approach to the analysis of brain structure based on the merging of concepts drawn from evolution and embryonic development.
Hodology
the study of connections within the central nervous system (‘odos’ is Greek for a road).
Neuromeres
transverse unitary

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