On the hodological criterion for homology

Abstract

Owen's pre-evolutionary definition of a homolog as “the same organ in different animals under every variety of form and function” and its redefinition after Darwin as “the same trait in different lineages due to common ancestry” entail the same heuristic problem: how to establish “sameness.”Although different criteria for homology often conflict, there is currently a generalized acceptance of gene expression as the best criterion. This gene-centered view of homology results from a reductionist and preformationist concept of living beings. Here, we adopt an alternative organismic-epigenetic viewpoint, and conceive living beings as systems whose identity is given by the dynamic interactions between their components at their multiple levels of composition. We posit that there cannot be an absolute homology criterion, and instead, homology should be inferred from comparisons at the levels and developmental stages where the delimitation of the compared trait lies. In this line, we argue that neural connectivity, i.e., the hodological criterion, should prevail in the determination of homologies between brain supra-cellular structures, such as the vertebrate pallium.

Hippocampal‐like circuitry in the pallium of an electric fish: Possible substrates for recursive pattern separation and completion

“…The authors concluded that, with the exception of the striatum and hippocampus, there are “traces of both molecular homoplasy and homology” and that “homology is not a dominant factor in their adult gene expression patterns.” A second approach (Puelles et al, ) emphasizes the developmental trajectory of pallium and cortex, e.g., “gene expression, neurogenetic timing, stratification patterns, invariant topology, radial vs. tangential migration” as a critical determinant of homology. Lastly, homology has been inferred from patterns of adult connectivity and function, as elegantly summarized by Karten () and Faunes et al (). The last approach reached very different conclusions from those of the first two approaches.…”

“…A second approach (Puelles et al, 2016) emphasizes the developmental trajectory of pallium and cortex, e.g., "gene expression, neurogenetic timing, stratification patterns, invariant topology, radial vs. tangential migration" as a critical determinant of homology. Lastly, homology has been inferred from patterns of adult connectivity and function, as elegantly summarized by Karten (2015) and Faunes et al (2015). The last approach reached very different conclusions from those of the first two approaches.…”

“…Based on striking similarities in the connectivity (laminar and columnar) and function of regions within the avian pallium and mammalian cortex, both authors concluded that, although their macroscopic organization is markedly different, there are precise homologies across avian pallium and mammalian cortex. Clearly, our comparison is primarily based on the pattern of connectivity and our hypothesis of homology between the DL/DDmg/P-intSS/DDi and DG/mossy cells/hilar SS cells/CA3 circuits is dependent on the same arguments (although with less data) as presented by Karten (2015) and Faunes et al (2015). A remarkable recent book (Wagner, 2014) offers a fresh look at this difficult problem based on in silico experiments on evolution; here we Hippocampal-like circuitry in the pallium The Journal of Comparative Neurology | Research in Systems Neuroscience present a highly simplified summary of the author's complicated arguments.…”

Orthogonal topography in the parallel input architecture of songbird HVC

“…Although avian cortical regions lack the distinctive Nissl‐defined laminar and columnar organization characteristic of most regions of mammal cortex, hodological analysis is leading to a new assessment of avian/mammal homologies at the level of neural connectivity (Faunes, Francisco Botelho, Ahumada Galleguillos, & Mpodozis, ; Karten, ). In this regard, the circuitry shown in Figure may begin to bring the connectivity of avian vocal‐motor networks into line with the connectivity of primate motor‐cortical networks (which were detected using similar retrograde tracing methods—Dea, Hamadjida, Elgbeili, Quessy, & Dancause, ; Hamadjida, Dea, Deffeyes, Quessy, & Dancause, ; Stepniewska, Preuss, & Kaas, ).…”

Morphological evolution of the vertebrate forebrain: From mechanical to cellular processes

“…A renewed version of the DVR-neocortex homology hypothesis has been supported by recent findings revealing that neurons in distinct laminae of the mammalian neocortex display similar microcircuitry and molecular markers as those observed in different components of the DVR and in the dorsal cortex/Wulst of sauropsids (Ahumada-Galleguillos, Fernández, Marin, Letelier, & Mpodozis, 2015;Briscoe & Ragsdale, 2018aDugas-Ford, Rowell, & Ragsdale, 2012;Faunes, Botelho, Ahumada Galleguillos, & Mpodozis, 2015;Fredes, Tapia, Letelier, Marín, & Mpodozis, 2010). This interpretation asserts that there are homologous neuronal populations in both structures so that the same canonical input-output processing microcircuit was present in the amniote last-common ancestor and was allocated to the mammalian neocortex and to the sauropsid DVR and dorsal cortex/Wulst (Briscoe & Ragsdale, 2018b).…”