Anatomical organization of the visual dorsal ventricular ridge in the chick (Gallus gallus): Layers and columns in the avian pallium

Abstract

The dorsal ventricular ridge (DVR) is one of the main components of the sauropsid pallium. In birds, the DVR is formed by an inner region, the nidopallium, and a more dorsal region, the mesopallium. The nidopallium contains discrete areas that receive auditory, visual, and multisensory collothalamic projections. These nidopallial nuclei are known to sustain reciprocal, short-range projections with their overlying mesopallial areas. Recent findings on the anatomical organization of the auditory DVR have shown that these short-range projections have a columnar organization that closely resembles that of the mammalian neocortex. However, it is unclear whether this columnar organization generalizes to other areas within the DVR. Here we examine in detail the organization of the visual DVR, performing small, circumscribed deposits of neuronal tracers as well as intracellular fillings in brain slices. We show that the visual DVR is organized in three main laminae, the thalamorecipient nucleus entopallium; a dorsally adjacent nidopallial lamina, the intermediate nidopallium; and a contiguous portion of the ventral mesopallium, the mesopallium ventrale. As in the case of the auditory DVR, we found a highly topographically organized system of reciprocal interconnections among these layers, which was formed by dorsoventrally oriented, discrete columnar bundles of axons. We conclude that the columnar organization previously demonstrated in the auditory DVR is not a unique feature but a general characteristic of the avian sensory pallium. We discuss these results in the context of a comparison between sauropsid and mammalian pallial organization.

Intratelencephalic projections of the avian visual dorsal ventricular ridge: Laminarly segregated, reciprocally and topographically organized

“…These cells were specifically codistributed with the field of terminals resulting from each of the injections, evidencing the topographic and reciprocal organization of the projections between the E and the M (Figure d,f). Furthermore, there were abundant terminal processes in the NI, confirming the existence of robust projections from the E and the MV onto the NI, as described previously by other authors (Ahumada‐Galleguillos et al, ; Husband & Shimizu, ; Tömböl et al, ). Lastly, as a result of both injections, there were substantial and rather extended axonal terminations into the underlying LSt (Figure c) as described previously (Ahumada‐Galleguillos et al, ; Krützfeldt & Wild, ).…”

“…We first sought to establish to what extent the visual DVR of pigeons is organized as previously described in chickens by Ahumada‐Galleguillos et al (). We addressed this issue by combining classic cytoarchitecture methods with in vivo tracing experiments.…”

“…They found that this region is constituted as a complex of laminarly arranged cell groups reciprocally interconnected by discrete columnar bundles of axons oriented perpendicular to the laminae, an arrangement that bears striking resemblance with that of the mammalian auditory cortex at laminar, cellular, and intrinsic circuitry levels. Subsequently, the organization of the visual DVR was addressed in detail by Ahumada‐Galleguillos, Fernández, Marin, Letelier, and Mpodozis (). According to these authors, this region can be regarded as a complex composed of three main layers: an internal nidopallial region, the entopallium (E), in receipt of very dense afferents from the thalamic stage of the tectofugal visual system, the nucleus rotundus (Rt); an overlying nidopallial layer, the intermediate nidopallium (NI), and the portion of the ventral division of the mesopallium located above the NI, the mesopallium ventrale (MV).…”

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).…”

Is Cetacean Intelligence Special? New Perspectives on the Debate

“…Moreover, the typical laminar organisation of the mammalian cortex (or the dorsal pallium in amphibians) is not as obvious in bird or reptile DVR since it is mainly a nuclear structure (i.e., large clusters of very densely packed neurons), although these nuclear clusters of neurons are homologous to lamina-specific populations of the mammalian cerebral cortex [33,34,36,60]. Furthermore, the characteristic laminar organisation that is seen in the cerebral cortex of mammals is also observed in the DVR's principal sensory zones [13,61]. Pigeons, for instance, have at least six distinct visual areas within their DVR, whereas turtles and lizards only possess between one and three [62][63][64].…”