Laminar and columnar auditory cortex in avian brain

Abstract

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 ...

From sauropsids to mammals and back: New approaches to comparative cortical development

“…While these divisions share a common basic plan at early developmental stages, later developmental programs trigger differential gene expression, neurogenetic patterns (Tsai et al, 1981; Nomura et al, 2013), lamination (Medina and Reiner, 2000), connectivity (Aboitiz et al, 2002; Karten, 2013), and cytoarchitecture (Wang et al, 2010) for each brain compartment. Diversification of the adult brain in gene expression and morphology across vertebrate phylogeny makes comparisons difficult (Aboitiz and Montiel, 2007; Wang et al, 2011a; Belgard and Montiel, 2013).…”

“…Cell groups are instead organized into nuclear‐like regions and are considered by some as a pseudolayered (columnar) organization (Medina and Reiner, 2000; Wang et al, 2010; Jarvis et al, 2013; Karten, 2013). Further, the hyperpallial layers are generally arranged parallel to the orientation of radial glial fibers, in striking contrast to the mammalian neocortical layers, which develop perpendicular to the orientation of radial glial fibers (as shown in Figs.…”

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

“…The AFP indirectly connects the song premotor cortical analog HVC (HVC is used as its proper name) and the song motor cortical analog RA (robust nucleus of the arcopallium) via the basal ganglia (striato-pallidal) nucleus Area X, the thalamus, and the prefrontal cortical analog LMAN (lateral magnocellular nucleus of the nidopallium) [see Fig. 1A for specific parallels to mammals; although these parallels are not complete (11,12), for simplicity we hereafter refer to LMAN as cortical]. As in mammals, the AFP is not required for the production of well-learned behaviors, but it is critically important for motor plasticity (13)(14)(15)(16)(17)(18).…”

Computation in networks

“…Some good references here are (Farris and Sinakevitch 2003) (basic theoretical background), (Sjöholm et al 2005) (very good on mushroom body discussions) and (Haehnel and Menzel 2010). Also, birds have an analogue of prefrontal cortex which is useful to think about: see (Herrold et al 2011) and (Wang et al 2010). The point here is that trying to answer high level questions about how a neural system leads to behavior and some level of cognition (again useful for autonomous robotics) can be helped by looking at other models.…”