Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns

Abstract

The last two authors contributed equally in co-supervising the project and conducting experiments. The second and last authors began this project originally as part of their graduate theses. ROLE OF AUTHORSEDJ, CCC, and KW performed experiments, quantifications, analyses, and wrote the article; JY, AP, CCC performed the computational analyses; MVR, HH, GF, OW, SCJ, ERJ, LK, SB, and ME performed gene expression experiments. SCJ also generated the 3D images and movies. AEPP processed and quantified images. CS and EH processed tissues and performed cell density measurements. HM helped co-supervise experiments.Additional Supporting Information may be found in the online version of this article. Detailed histological data from this article are available as virtual slides or whole-slide images using Biolucida Cloud image streaming technology from MBF Bioscience. The collection can be accessed at http://Wiley.Biolucida.net/JCN521-16Jarvis_Chen. All supporting figures and videos are located at: https://www.dropbox.com/sh/hl97l6a5zzxo54o/0MVQw0_epr NIH Public Access AbstractBased on quantitative cluster analyses of 52 constitutively expressed or behaviorally regulated genes in 23 brain regions, we present a global view of telencephalic organization of birds. The patterns of constitutively expressed genes revealed a partial mirror image organization of three major cell populations that wrap above, around, and below the ventricle and adjacent lamina through the mesopallium. The patterns of behaviorally regulated genes revealed functional columns of activation across boundaries of these cell populations, reminiscent of columns through layers of the mammalian cortex. The avian functionally regulated columns were of two types: those above the ventricle and associated mesopallial lamina, formed by our revised dorsal mesopallium, hyperpallium, and intercalated hyperpallium; and those below the ventricle, formed by our revised ventral mesopallium, nidopallium, and intercalated nidopallium. Based on these findings and known connectivity, we propose that the avian pallium has four major cell populations similar to those in mammalian cortex and some parts of the amygdala: 1) a primary sensory input population (intercalated pallium); 2) a secondary intrapallial population (nidopallium/hyperpallium); 3) a tertiary intrapallial population (mesopallium); and 4) a quaternary output population (the arcopallium). Each population contributes portions to columns that control different sensory or motor systems. We suggest that this organization of cell groups forms by expansion of contiguous developmental cell domains that wrap around the lateral ventricle and its extension through the middle of the mesopallium. We believe that the position of the lateral ventricle and its associated mesopallium lamina has resulted in a conceptual barrier to recognizing related cell groups across its border, thereby confounding our understanding of homologies with mammals. INDEXING TERMSforebrain; brain pathways; brain organization; neural activity; motor b...

Birds have primate-like numbers of neurons in the forebrain

“…5 B-D), implying that parrots have evolved a specific, previously unrecognized cerebrotype (43) distinguished by a higher number of neurons allocated to the subpallium. Because subpallial structures play an important role in sensory and motor learning and execution of motor behavior (15,44), we suggest that the relatively enlarged subpallium in large parrots is likely associated with their greater learning skills, including vocal learning, and enhanced foot and beak dexterity (5, 6, 13, 45).…”

“…Avian brains thus have the potential to provide much higher "cognitive power" per unit mass than do mammalian brains. amygdala) (14)(15)(16)41). The avian subpallium (formed by the striatum, pallidum, and septum), diencephalon, tectum, and brainstem were pooled and compared with the same regions of mammalian brains that are referred to as "the rest of brain."…”

“…Superficially, the architecture of the avian brain appears very different from that of mammals, but recent work demonstrates that, despite a lack of layered neocortex, large areas of the avian forebrain are homologous to mammalian cortex (14-16), conform to the same organizational principles (15,17,18), and play similar roles in higher cognitive functions (14,19), including executive control (20,21). However, bird brains are small and the computational mechanisms enabling corvids and parrots to achieve ape-like intelligence with much smaller brains remain unclear.…”

Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds

“…Moreover, the two areas share important properties such as dense innervation by dopaminergic fibres and connectivity patterns with multiple sensory input, limbic and motor output regions 16 . However, the pattern of thalamic connections 22 as well as developmental gene expression patterns 23,24 and differences in macroarchitectures in birds versus mammals suggest that NCL and PFC are not homologous-that is, they independently evolved from different parts of the pallium 25,26 . Therefore, the avian NCL is considered to be a functional analogue of the mammalian PFC 14 , a structure with similar function but different evolutionary origin.…”

Differential Expression of Melatonin Receptor Subtypes MelIa, MelIb and MelIc in Relation to Melatonin Binding in the Male Songbird Brain

“…Thus, there are MelR-expressing brain areas which are not explicitly mentioned in the present work, in particular when expression is scattered. Anatomical descriptions were based on recent reviews of the nomenclature [Reiner et al, 2004;Chen et al, 2013;Jarvis et al, 2013].…”