The mammalian neocortex mediates complex cognitive behaviors, such as sensory perception, decision making, and language. The evolutionary history of the cortex, and the cells and circuitry underlying similar capabilities in nonmammals, are poorly understood, however. Two distinct features of the mammalian neocortex are lamination and radially arrayed columns that form functional modules, characterized by defined neuronal types and unique intrinsic connections. The seeming inability to identify these characteristic features in nonmammalian forebrains with earlier methods has often led to the assumption of uniqueness of neocortical cells and circuits in mammals. Using contemporary methods, we demonstrate the existence of comparable columnar functional modules in laminated auditory telencephalon of an avian species (Gallus gallus). A highly sensitive tracer was placed into individual layers of the telencephalon within the cortical region that is similar to mammalian auditory cortex. Distribution of anterograde and retrograde transportable markers revealed extensive interconnections across layers and between neurons within narrow radial columns perpendicular to the laminae. This columnar organization was further confirmed by visualization of radially oriented axonal collaterals of individual intracellularly filled neurons. Common cell types in birds and mammals that provide the cellular substrate of columnar functional modules were identified. These findings indicate that laminar and columnar properties of the neocortex are not unique to mammals and may have evolved from cells and circuits found in more ancient vertebrates. Specific functional pathways in the brain can be analyzed in regard to their common phylogenetic origins, which introduces a previously underutilized level of analysis to components involved in higher cognitive functions. neocortex evolution | columnar organization | primary auditory cortex | intrinsic circuitry | granule cell T he origins and evolution of the forebrain and the mammalian neocortex,* where complex cognitive functions are centered, have long been of broad interest to scientists and nonscientists alike. For more than 100 y, the neocortex was considered an independently evolved structure unique to mammals. The nonmammalian telencephalon was frequently compared with the mammalian basal ganglia, which was thought to be involved in stereotypical instinctive behaviors (1). A revolutionary revision in our concept of the nature of vertebrate brain organization was recently accepted in the revised nomenclature of the avian brain (2, 3). The avian Wulst and dorsal ventricular ridge, two prominent components of the telencephalon, are recognized as being homologous to pallial components of mammalian brains, which is consistent with the idea that avian telencephalon includes a large cortical component ( Fig. 1 A-C) (4-6). However, this postulated homology addresses only the most general aspects of the evolutionary relationship of the avian brain to the mammal brain, that is, in indicating that ...
We describe a set of new comprehensive, high-quality, high-resolution digital images of histological sections from the brain of male zebra finches (Taeniopygia guttata), and make them publicly available through an interactive website (http://zebrafinch.brainarchitecture.org/). These images provide a basis for the production of a dimensionally accurate and detailed digital non-stereotaxic atlas. Nissl- and myelin-stained brain sections are provided in the transverse, sagittal, and horizontal planes, with the transverse plane approximating the more traditional Frankfurt Plane. In addition, a separate set of brain sections in this same plane is stained for tyrosine hydroxylase, revealing the distribution of catecholaminergic neurons (dopaminergic, noradrenergic, and adrenergic) in the songbird brain. For a subset of sagittal sections we have also prepared a corresponding set of drawings, defining and annotating various nuclei, fields, and fiber tracts that are visible under Nissl and myelin staining. This atlas of the zebra finch brain is expected to become an important tool for birdsong research and comparative studies of brain organization and evolution.
The possibility that GABA-like immunoreactive cells of the chick retina also contain neuronal nicotinic acetylcholine receptors was investigated by means of immunohistochemical techniques. Double-labeled cell bodies containing GABA-like immunoreactivity and nicotinic receptor-like immunoreactivity were seen in the inner third of the inner nuclear layer and were presumably amacrine cells. Approximately 29-36% of the GABA-positive cells in the inner nuclear layer contained nicotinic receptor immunoreactivity. Their soma sizes ranged from 5-12 microns. Some double-labeled cells ranging from 7-21 microns were observed in the ganglion cell layer as well. Between 9-37% of the GABA-positive cells in this layer contained nicotinic receptor-like immunoreactivity. Following injection of a retrograde tracer into the optic tectum, some of the retrogradely labeled cells were also double labeled with antibodies against GABA and nicotinic receptors. This indicates that at least some of the GABA-positive cells containing nicotinic acetylcholine receptors in the ganglion cell layer are indeed ganglion cells. The present data appear to represent the first demonstration of the presence of acetylcholine receptors in GABA-containing cells in the retina, thus providing a basis for a possible influence of acetylcholine upon those presumptive GABAergic cells.
Two cDNA clones for nicotinic acetylcholine receptor (nAChR) subunits sensitive to a-bungarotoxin (a-Bgt) have been isolated, the so-called a-Bgt binding proteins al (or a7 nAChR subunit) and a2 (or a8 nAChR subunit). Immunohistochemical experiments have shown that both a7 and a8 subunits, as well as subunits insensitive to a-Bgt (j32 and a3), are present in amacrine and ganglion cells of the chick retina. However, only the a8 subunit was observed in presumptive bipolar cells. The present study investigated in detail the pattern of distribution of the bipolar cells containing the a8 nAChR subunit and its relation to the pattern of distribution of bipolar cells immunoreactive to protein kinase C (PKC). Presumptive a8-and PKC-like immunoreactive (a8-LI and PKC-LI) bipolar cells were observed sending their dendrites to the outer plexiform layers and their axons to the inner plexiform layer. Whereas a8-LI bipolar cells corresponded to 40-53% of the whole population of bipolar cells, PKC-LI bipolar cells represented only 6-8% of the same population. The soma sizes of the a8-LI bipolar cells were slightly smaller (mean ± S.D.; 4.9 ± 0.8 /im) than the soma sizes of the PKC-LI bipolar cells (5.4 ± 0.9 fim). Double-labeling experiments indicated that probably all PKC-LI bipolar cells also contain a8-LI. This indicates that two distinct groups of cholinoceptive bipolar cells exist in the chick retina, one that contains PKC-LI, and another one that does not.
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