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A Cortex-Like Canonical Circuit in the Avian Forebrain the Processing of Stereopsis, Combined with High Visual Acuity in the Wulst of This Species

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A Cortex-Like Canonical Circuit in the Avian Forebrain the Processing of Stereopsis, Combined with High Visual Acuity in the Wulst of This Species RESEARCH ◥ both species showed a comparable column- RESEARCH ARTICLE SUMMARY and lamina-like circuit organization, small species differences were discernible, particu- NEUROSCIENCE larly for the Wulst, which was more subdif- ferentiated in barn owls, which fits well with A cortex-like canonical circuit in the avian forebrain the processing of stereopsis, combined with high visual acuity in the Wulst of this species. Martin Stacho*†, Christina Herold†, Noemi Rook, Hermann Wagner, Markus Axer, The primary sensory zones of the DVR were Katrin Amunts, Onur Güntürkün tightly interconnected with the intercalated nidopallial layers and the overlying meso- pallium. In addition, nidopallial and some INTRODUCTION: For more than a century, the radial and tangential directions. These fibers hyperpallial lamina-like areas gave rise to long- avian forebrain has been a riddle for neurosci- constitute repetitive canonical circuits as compu- range tangential projections connecting sen- entists. Birds demonstrate exceptional cogni- tational units that process information along sory, associative, and motor structures. tive abilities comparable to those of mammals, the radial domain and associate it tangentially. but their forebrain organization is radically In this study, we first analyzed the pallial fiber CONCLUSION: Our study reveals a hitherto un- different. Whereas mammalian cognition architecture with three-dimensional polarized known neuroarchitecture of the avian sensory emerges from the canonical circuits of the six- light imaging (3D-PLI) in pigeons and subse- forebrain that is composed of iteratively or- layered neocortex, the avian forebrain seems quently reconstructed local sensory circuits ganized canonical circuits within tangentially to display a simple nuclear organization. Only of the Wulst and the sensory DVR in pigeons organized lamina-like and orthogonally posi- Downloaded from one of these nuclei, the Wulst, has been gen- and barn owls by means of in vivo or in vitro tioned column-like entities. Our findings suggest erally accepted to be homologous to the applications of neuronal tracers. We focused that it is likely that an ancient microcircuit that neocortex. Most of the remaining pallium is on two distantly related bird species to prove already existed in the last common stem am- constituted by a multinuclear structure called the hypothesis that a canonical circuit com- niote might have been evolutionarily conserved the dorsal ventricular ridge (DVR), which has parable to the neocortex is a genuine feature and partly modified in birds and mammals. The no direct counterpart in mammals. Neverthe- of the avian sensory forebrain. avian version of this connectivity blueprint could http://science.sciencemag.org/ less, one long-standing theory, along with re- conceivably generate computational properties cent scientific evidence, supports the idea that RESULTS: The 3D-PLI fiber analysis showed that reminiscent of the neocortex and would thus some parts of the sensory DVR could display both the Wulst and the sensory DVR display provide a neurobiological explanation for the connectivity patterns, physiological signatures, an orthogonal organization of radially and tan- comparable and outstanding perceptual and and cell type–specific markers that are remi- gentially organized fibers along their entire cognitive feats that occur in both taxa.▪ niscent of the neocortex. However, it remains extent. In contrast, nonsensory components unknown if the entire Wulst and sensory DVR of the DVR displayed a complex mosaic-like The list of author affiliations is available in the full article online. harbor a canonical circuit that structurally re- arrangement with patches of fibers with dif- *Corresponding author. Email: [email protected] sembles mammalian cortical organization. ferent orientations. Fiber tracing revealed an †These authors contributed equally to this work. Cite this article as M. Stacho et al., Science 369, eabc5534 iterative circuit motif that was present across (2020). DOI: 10.1126/science.abc5534 on September 24, 2020 RATIONALE: The mammalian neocortex com- modalities (somatosensory, visual, and audi- prises a columnar and laminar organization tory), brain regions (sensory DVR and Wulst), READ THE FULL ARTICLE AT with orthogonally organized fibers that run in and species (pigeon and barn owl). Although https://doi.org/10.1126/science.abc5534 Rat brain Pigeon brain Visual ry Somatosensory ito Visual NC AuditoryAud Motor Wulst Visual Somato- sensory Prefrontal Neocortex nal VV/VI/VI I IVV I II/IIII/III/III gemi AudAAuditoryuddititotory TrigeminalTri Arcopallium Neocortical DVR layers Subpallium Subpallium Fiber architectures of mammalian and avian forebrains. Schematic drawings this study, both mammals and birds show an orthogonal fiber architecture of a rat brain (left) and a pigeon brain (right) depict their overall pallial constituted by radially (dark blue) and tangentially (white) oriented fibers. organization. The mammalian dorsal pallium harbors the six-layered neocortex Tangential fibers associate distant pallial territories. Whereas this pattern with a granular input layer IV (purple) and supra- and infragranular layers II/III dominates the whole mammalian neocortex, in birds, only the sensory DVR and and V/VI, respectively (blue). The avian pallium comprises the Wulst and the the Wulst (light green) display such an architecture, and the associative and DVR, which both, at first glance, display a nuclear organization. Their primary motor areas (dark green), as in the caudal DVR, are devoid of this cortex-like 3D RAT BRAIN (LEFT): SCALABLE BRAIN ATLAS,sensory RESEARCH RESOURCE IDENTIFIER (RRID) SCR_006934 input zones are shown in purple, comparable to layer IV. According to fiber architecture. NC, caudal nidopallium. Stacho et al., Science 369, 1585 (2020) 25 September 2020 1of1 RESEARCH ◥ key, and human and compared them to their RESEARCH ARTICLE avian homologous counterpart, the visual Wulst of the pigeon (Fig. 1). In all four brains, NEUROSCIENCE we detected a high prevalence of radially ori- ented fibers crossed by tangential fibers in A cortex-like canonical circuit in the avian forebrain some layers. The visibility of tangential fibers differed notably between the mammalian spe- Martin Stacho1,2*†, Christina Herold3†, Noemi Rook1, Hermann Wagner4, Markus Axer5, cies but included superficial layers I to III, deep Katrin Amunts3,5, Onur Güntürkün1 layers V and VI, and layer IVb in mammals, as well as the hyperpallium densocellulare (HD), Although the avian pallium seems to lack an organization akin to that of the cerebral cortex, birds the hyperpallium apicale (HA), and the inter- exhibit extraordinary cognitive skills that are comparable to those of mammals. We analyzed the fiber stitial part of the hyperpallium apicale (IHA) architecture of the avian pallium with three-dimensional polarized light imaging and subsequently in pigeons. The predominance of radial fibers reconstructed local and associative pallial circuits with tracing techniques. We discovered an iteratively was also layer and species specific. In the rat repeated, column-like neuronal circuitry across the layer-like nuclear boundaries of the hyperpallium and the vervet monkey brains, the radial fibers and the sensory dorsal ventricular ridge. These circuits are connected to neighboring columns and, via were particularly visible between layers II and tangential layer-like connections, to higher associative and motor areas. Our findings indicate that IV, whereas the human cortex displayed the this avian canonical circuitry is similar to its mammalian counterpart and might constitute the structural most radial fibers between layers IIIb and VI. basis of neuronal computation. In the vervet brain, layer IV showed very clear subdifferentiations based on the preponder- Downloaded from ance of tangential and radial fibers; while the ammals and birds share a common scending cortical pathways (6, 11). The local radial fibers were visible in layer IVc, they were ancestor that lived ~320 million years connectivity patterns of auditory and visual suspended by tangential fibers in layer IVb ago. Since then, this ancestor’sdorsal DVR areas were also shown to display layer- and became visible again from the adjacent pallium has developed into the cerebral and column-like connectivity (12–14). These layer IVa to superficial layer II (Fig. 1C, and M http://science.sciencemag.org/ cortex in the mammalian lineage. The latter findings suggest the possibility that at see below). cortex is composed of cortical layers running least some DVR components could display a parallel to the cortical surface, as well as col- cortex-like architecture. The overall fiber architecture of the avian umns that run orthogonal to layers and thus We thus asked three questions: (i) Does a sensory pallium create a radial organization (1, 2). Cortical lay- microscale fiber architecture analysis of the We first analyzed the overall fiber architec- ers contain different types of neurons, each entire avian sensory DVR and the hyperpal- ture in pigeons, starting with the DVR using with specific afferent and efferent connections lium reveal a cortex-like pattern of radially and 3D-PLI (Fig. 1 and fig. S1) (19, 20). The DVR (2, 3). Layers and columns show a character- tangentially organized fiber units? (ii) Are the harbors three primary sensory territories, which istic pattern in each cortical area, which is local connectivity patterns of these layer- and (from anterior to posterior) are
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