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

Abstract

Recent reports have shown that the avian visual dorsal ventricular ridge (DVR) is organized as a trilayered complex, in which the forming layers—the thalamo‐recipient entopallium (E), an overlaying nidopallial stripe called intermediate nidopallium (NI), and the dorsally adjacent mesopallium ventrale—appear to be extensively interconnected by topographically organized columns of reciprocal axonal processes running perpendicular to the layers, an arrangement highly reminiscent to that of the sensory cortices of mammals. In the present report, we implemented in vivo anterograde and retrograde tracing techniques aiming to elucidate the organization of the connections of this complex with other pallial areas. Previous studies have shown that the efferent projections of the visual DVR originate mainly from the NI and E, reaching several distinct associative and premotor nidopallial areas. We found that the efferents from the visual DVR originated solely from the NI, and confirmed that the targets of these projections were the pallial areas described by previous studies. We also found novel projections from the NI to the visual hyperpallium, and to the lateral striatum. Moreover, we found that these projections were reciprocal, topographically organized, and originated from different cell populations within the NI. We conclude that the NI constitutes a specialized layer of the visual DVR that form the core of a dense network of highly specific connections between this region and other higher order areas of the avian pallium. Finally, we discuss to what extent these hodological properties resemble those of the mammalian cortical layers II/III.

A canonical interlaminar circuit in the sensory dorsal ventricular ridge of birds: The anatomical organization of the trigeminal pallium

“…Finally, it is worth noting that in the sagittal plane used in this study all major sensory areas of the DVR, as well as its forming sensory layer‐like partitions (as described previously by Ahumada‐Galleguillos et al, 2015; Fernández, Ahumada‐Galleguillos, et al, 2020; Jarvis et al, 2013), can be appreciated in a rostro‐caudal continuity in EAG2 in situ hybridization preparations. In this preparation, each and all of the senso‐recipient layers of the DVR display substantial numbers of EAG2 positive somata (Figure 3).…”

“…A prominent feature of the amniote pallial telencephalon is the presence of specialized areas receiving ascending projections from different sensory modalities (Buttler & Hodos, 2005). In mammals, these ascending sensory pathways innervate distinct regions of the dorsolateral pallium, which is elaborated as a six-layered cortex in these vertebrates (Fernandez et al, 1998;Puelles, 2001;Puelles et al, 2000;Striedter, 1997). In birds, most of these sensory pathways innervate different areas of the ventro-lateral pallium, which is formed by a set of prominent nuclear-like divisions protruding into the ventricle, together termed dorsal ventricular ridge (DVR; Dubbeldam, 1998;Karten, 1969).…”

“…In this regard, recent anatomical studies of the auditory and visual areas of the DVR have shown that, in spite of mediating different sensory modalities, these areas share a common, highly elaborated pattern of internal connectivity. Specifically, both these regions appear organized as complexes of laminarly arranged cell groups highly interconnected in a “laminar/columnar” fashion, in such a way that cells located in homotopic positions in each of the forming layers (senso‐recipient nidopallium, intermediate nidopallium, and ventral mesopallium) are reciprocally linked by a local loop of axonal processes running across these layers (Ahumada‐Galleguillos et al, 2015; Fernández, Ahumada‐Galleguillos, et al, 2020; Wang et al, 2010). Interestingly, such laminar/columnar arrangement bears a striking resemblance to that of the mammalian sensory cortices at laminar, cellular and intrinsic circuitry levels (Dugas‐Ford et al, 2012; Faunes et al, 2015; Jarvis et al, 2013; Karten, 2015; Stacho et al, 2020).…”

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia)

“…Previous works suggested that the NI (considered as Ep and Ep2) projection to the lateral pallium was segregated in the anterior–posterior axis, such that the anterior NI projected to the NFL, the central NI to the NIL, and the posterior NI to the NCL (Husband & Shimizu, ). However, Fernández et al () have shown that the entire NI projects to each of its targets including the mentioned nidopallial areas and the Arc, and therefore, a complete representation of the Rt subdivisions should be expected in all structures. Nonetheless, in accordance with Husband and Shimizu (), Fernández et al () also found that the RtDa‐related zone in the anterior NI projects more densely to the NFL than to the NCL.…”

“…However, Fernández et al () have shown that the entire NI projects to each of its targets including the mentioned nidopallial areas and the Arc, and therefore, a complete representation of the Rt subdivisions should be expected in all structures. Nonetheless, in accordance with Husband and Shimizu (), Fernández et al () also found that the RtDa‐related zone in the anterior NI projects more densely to the NFL than to the NCL. In addition, the RtCe projection seems to be heavily oriented to the striatum, which may thus leave a weak representation of this division in the NI.…”