Molecular architecture of the zebra finch arcopallium

Abstract

The arcopallium, a key avian forebrain region, receives inputs from numerous brain areas and is a major source of descending sensory and motor projections. While there is evidence of arcopallial subdivisions, the internal organization or the arcopallium is not well understood. The arcopallium is also considered the avian homologue of mammalian deep cortical layers and/or amygdalar subdivisions, but one‐to‐one correspondences are controversial. Here we present a molecular characterization of the arcopallium in the zebra finch, a passerine songbird species and a major model organism for vocal learning studies. Based on in situ hybridization for arcopallial‐expressed transcripts (AQP1, C1QL3, CBLN2, CNTN4, CYP19A1, ESR1/2, FEZF2, MGP, NECAB2, PCP4, PVALB, SCN3B, SCUBE1, ZBTB20, and others) in comparison with cytoarchitectonic features, we have defined 20 distinct regions that can be grouped into six major domains (anterior, posterior, dorsal, ventral, medial, and intermediate arcopallium, respectively; AA, AP, AD, AV, AM, and AI). The data also help to establish the arcopallium as primarily pallial, support a unique topography of the arcopallium in passerines, highlight similarities between the vocal robust nucleus of the arcopallium (RA) and AI, and provide insights into the similarities and differences of cortical and amygdalar regions between birds and mammals. We also propose the use of AMV (instead of nucleus taenia/TnA), AMD, AD, and AI as initial steps toward a universal arcopallial nomenclature. Besides clarifying the internal organization of the arcopallium, the data provide a coherent basis for further functional and comparative studies of this complex avian brain region.

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

“…In mammals, these nuclei are specifically targeted by neurons from cortical layer V. Like layer V neurons, the AI also gives rise to long‐range descending projections to the midbrain tectum and tegmentum, as well as to the lateral pons. Furthermore, recent receptor and gene expression studies have shown a close similarity between regions of the arcopallium, including AI, and cortical layer V–VI cell populations (Chen et al, ; Dugas‐Ford et al, ; Jarvis et al, ; Mello et al, ; Pfenning et al, ).…”

“…(Atoji, Saito, & Wild, 2006;Cohen, 1975;Herold, Paulitschek, Palomero-Gallagher, Güntürkün, & Zilles, 2018;Jarvis et al, 2005;Jarvis et al, 2013;Kröner & Güntürkün, 1999;Reiner et al, 2004;Schriber, 1978;Veenman, Wild, & Reiner, 1995;Wynne & Güntürkün, 1995). An additional ventral arcopallial division (AV) combines "viscerolimbic" molecular characteristics with connectional properties related to sensory, associative processing (Herold et al, 2018;Mello, Kaser, Buckner, Wirthlin, & Lovell, 2019;Shanahan et al, 2013).…”

Multi-dimensional tuning in motor cortical neurons during active behavior

“…We found that most AId neurons were selective for single movements or for different AId of anesthetized zebra finches elicits increased spontaneous firing rates, and parvalbumin expression is higher in AId compared to surrounding motor cortex (Mello et al, 2019;Yuan and Bottjer, 2019). Similarly, mammalian motor cortex contains a substantial population of inhibitory interneurons, which have been implicated in both regulating plasticity during motor skill learning and coordinating activity across motor cortex during behavior (Jacobs and Donoghue, 1991;Hess and Donoghue, 1994;Hess et al, 1996;Markram et al, 2004;Stagg et al, 2011;Donato et al, 2013;Chen et al, 2015;Kida et al, 2016;Adler et al, 2019).…”

Molecular specializations of deep cortical layer analogs in songbirds

“…The RA is considered part of the intermediate arcopallium, which is the major source of descending output from the avian telencephalon 38 . The arcopallium, more broadly, is thought to contain the avian analog of the deep layers of the mammalian sensory and motor cortices based on similarities in their projection patterns 31 , 39 , neuronal activation 33 , 40 , and transcriptional profiles 41 – 44 , but may also contain the avian equivalent of pallial parts of the mammalian amygdala 44 – 46 . Avian analogs of RA are found in other birds that evolved vocal learning 9 – 13 , but are thought to be absent in vocal non-learning birds based on cytoarchitectonics and molecular criteria 14 – 16 , 47 ; but see also 17 , 18 .…”