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 ...

The nucleus isthmi pars magnocellularis (Imc) and pars parvocellularis (Ipc) influence the receptive field structure of neurons in the optic tectum (TeO). To understand better the anatomical substrate of isthmotectal interactions, neuronal morphology and connections of Imc were examined in chicks (Gallus gallus). Cholera toxin B injection into TeO demonstrated a coarse topographical projection from TeO upon Imc. Retrogradely labeled neurons were scattered throughout Imc and in low density within the zone of anterogradely labeled terminals, suggesting a heterotopic projection from Imc upon TeO. This organization differed from the precise homotopic reciprocal connections of Ipc and the nucleus isthmi pars semilunaris (SLu) with TeO. By using slice preparations, extracellular biotinylated dextran amine injections demonstrated a dense projection from most neurons in Imc upon both Ipc and SLu. Intracellular filling of Imc neurons with biocytin revealed two cell types. The most common, Imc-Is, formed a widely ramifying axonal field in both Ipc and SLu, without obvious topography. A less frequently observed cell type, Imc-Te, formed a widely ramifying terminal field in layers 10-12 of TeO. No neurons were found to project upon both Ipc/SLu and TeO. Both types possessed local axon collaterals and flat dendritic fields oriented parallel to the long axis of Imc. Imc neurons contain glutamic acid decarboxylase, which is consistent with Imc participating in center-surround or other wide-field inhibitory isthmotectal interactions. The laminar and columnar pattern of isthmotectal terminals also suggests a means of interacting with multiple tectofugal pathways, including the stratified subpopulations of tectorotundal neurons participating in motion detection.

The cholinergic division of the avian nucleus isthmi, the homolog of the mammalian nucleus parabigeminalis, is composed of the pars parvocellularis (Ipc) and pars semilunaris (SLu). Ipc and SLu were studied with in vivo and in vitro tracing and intracellular filling methods. 1) Both nuclei have reciprocal homotopic connections with the ipsilateral optic tectum. The SLu connection is more diffuse than that of Ipc. 2) Tectal inputs to Ipc and SLu are Brn3a-immunoreactive neurons in the inner sublayer of layer 10. Tectal neurons projecting on Ipc possess "shepherd's crook" axons and radial dendritic fields in layers 2-13. 3) Neurons in the mid-portion of Ipc possess a columnar spiny dendritic field. SLu neurons have a large, nonoriented spiny dendritic field. 4) Ipc terminals form a cylindrical brush-like arborization (35-50 microm wide) in layers 2-10, with extremely dense boutons in layers 3-6, and a diffuse arborization in layers 11-13. SLu neurons terminate in a wider column (120-180 microm wide) lacking the dust-like boutonal features of Ipc and extend in layers 4c-13 with dense arborizations in layers 4c, 6, and 9-13. 5) Ipc and SLu contain specialized fast potassium ion channels. We propose that dense arborizations of Ipc axons may be directed to the distal dendritic bottlebrushes of motion detecting tectal ganglion cells (TGCs). They may provide synchronous activation of a group of adjacent bottlebrushes of different TGCs of the same type via their intralaminar processes, and cross channel activation of different types of TGCs within the same column of visual space.