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Uncovering organizational principles of the cerebral cortex is essential for proper understanding of this prominent structure of the mammalian brain. The theory of the dual origin of the cerebral cortex offers such organizational principle. Here, we demonstrate that a duality pertains to the connectional architecture of the cerebral cortex of different mammals. This dual structure also constitutes a major axis of organization of the transcriptional architecture of the cortex and reflects the expression of different morphogens stemming from distinct patterning centers in the developing pallium. The duality of the cortex is also reflected in its spatial dimension, highlighting cortical areas as spatially ordered constellations that are centered around the paleocortex and archicortex, with the later primordial moieties reminiscent of antipodal points in the cortical sheet. The ontogeny of the uncovered dual connectional structure might be rooted in heterochronous neurodevelopmental gradients in the developing pallium, a suggestion corroborated by computational modeling. In all, the current results exemplify the duality of the cerebral cortex as an overarching organizational principle, reflected across the different levels of cortical architecture of different mammalian species, defining a natural axis of mammalian cortical organization.

In the last few years, several studies have revisited long-held assumptions in the field of brain development and evolution providing us with a fundamentally new vision on the mechanisms controlling its size and shape, hence function. Among these studies, some described hitherto unforeseeable subtypes of neural progenitors while others reinterpreted long-known observations about their cell cycle in alternative new ways. Most remarkably, this knowledge combined has allowed the generation of mammalian model organisms in which brain size and folding has been selectively increased giving us the means to understand the mechanisms underlying the evolution of the most complex and sophisticated organ. Here we review the key findings made in this area and make a few conjectures about their evolutionary meaning including the likelihood of Martians conquering our planet., VB and FC are supported by the Ministerio de Economía y Competitividad (BFU2012-33473) and European Research Council (309633) (VB), DFG Collaborative Research Center SFB655, Center for Regenerative Therapies and Medical Faculty of the TU–Dresden (FC).

The developmental principles that establish the columnar edifice of the cerebral cortex underlie its evolution and dictate its physiological operations and cognitive capacity. This article contrasts the initial discoveries made by Ramón y Cajal and his contemporaries, based on the ingenious interpretation of neuronal shapes and their relationships using the Golgi method, with new insights based on the application of the most advanced methods of molecular biology and genetics. We can now propose a realistic model of how the sequence of gene expression, cascade of multiple molecular pathways and cell-cell interactions establish the number of neurons, guide their migration and allocation into proper regions and determine their differentiation into specific phenotypes that establish specific synaptic connections. The findings obtained from different levels of analyses sustain the radial unit hypothesis as a useful framework for understanding the mechanisms of cortical development and its evolution as an organ of thought.

According to the structural model of prefrontal cortex, the pattern of corticocortical connections is intricately linked to cortical architecture (Cereb. Cortex 7 (1997) 635). We further explored this model by using quantitative methods to describe the structure and connections of prefrontal cortices. Multi-parameter analyses distinguished different cortical types, positioning at one extreme medial and orbitofrontal (limbic) cortices, and at the other extreme, lateral (eulaminate) cortices. The structural model accurately predicted the laminar pattern of connections, and the relative distribution of connections within cortical layers, based on cortical type. This model may provide the foundation to predict the nature of corticocortical processing and its disruption in psychiatric and neurologic diseases, where neuropathology affects specific types of neurons and layers.

We present a model of a cortical-type architecture that uses a latency coding scheme to process inputs as fast as possible given certain neuronal constraints while at the same time keeping the potential to perform a detailed analysis. The basic processing elements of our network are columnar structures, called minicolumns. We propose that these minicolumns are the prime constituents of cortical architecture.

While many models of the dynamics and interactions of single neurons are extant, analogous constructs which attempt to describe large-scale (≥O(108)) neuronal activity are few and far between. Optical imaging of the visual cortex makes such macroscopic neuronal activity accessible. Symmetries latent in the cortical architecture are used here to develop a scheme for analyzing such images. In this way, intrinsic modes of cortical response can be uncovered, using minimal assumptions. Some of these modes correspond to already-familiar features of the functional architecture, and it is highly likely that others hold physiological relevance as well. Finally, the number of such modes that would be required in a more fully developed model (incorporating cortical dynamics) is approximated.

In modern computer design considerable care is taken to arrange the components in such a way that wiring is kept to a minimum. Certain features of cortical structure — the mappings, stripes and blobs within areas, and areas themselves — are somewhat reminiscent of the layout of computer components, and suggest that the cortex may also be organized so as to economize on neuronal ‘wiring'. One important difference between the brain and a computer is that the wiring in the brain takes the form of elaborate branched structures, namely axonal trees. In this article, it is argued that an assessment of the efficiency of cortical wiring must take account of the branching rules of these trees.

Scalp responses evoked by patterned visual stimuli and by changes in luminance were recorded both from human subjects and monkeys. Three models are proposed to explain the observed stimulus-response relations: 1. (1) Luminance detection by first order summing units. 2. (2) A centre-surround antagonistic mechanism which enhances responses to spatial patterning. 3. (3) Contour detection by ordered arrays of overlapping receptive fields. Implications of the three hypotheses are discussed. Experimental evidence is presented which shows that a definite contour-specific response component can be observed in most human subjects. Spatial frequency selectivity by centre-surround antagonism seems the most plausible explanation of our results in monkey. The differences between human and monkey stimulus-response relationships are tentatively explained by the differences in cortical architecture, assuming the origin of spatial frequency selectivity in striate cortex and, in accordance with Michael and Halliday (1971) and Jeffreys (1971), a mainly extrastriate origin of the specific contour response.