Recent studies have revealed marked variation in pyramidal cell structure in the visual cortex of macaque and marmoset monkeys. In particular, there is a systematic increase in the size of, and number of spines in, the arbours of pyramidal cells with progression through occipitotemporal (OT) visual areas. In the present study we extend the basis for comparison by investigating pyramidal cell structure in OT visual areas of the nocturnal owl monkey. As in the diurnal macaque and marmoset monkeys, pyramidal cells became progressively larger and more spinous with anterior progression through OT visual areas. These data suggest that: 1. the trend for more complex pyramidal cells with anterior progression through OT visual areas is a fundamental organizational principle in primate cortex; 2. areal specialization of the pyramidal cell phenotype provides an anatomical substrate for the reconstruction of the visual scene in OT areas; 3. evolutionary specialization of different aspects of visual processing may determine the extent of interareal variation in the pyramidal cell phenotype in different species; and 4. pyramidal cell structure is not necessarily related to brain size.

The three-dimensional structure of Golgi-impregnated neurons was studied using modern data collecting techniques. Branch length and branch angle distributions of the bifurcating dendritic structure were examined and found to have a wide continuous range of observed values. These types of distributions imply a stochastic design for the bifurcating structure. No apparent pattern was found in the branching configuration. However more work is needed to examine all possible correlations between the observed classes of measured values. Basal dendrites seem to follow the same stochastic branching pattern where branch segment distributions even have the same parameters. However, some basal dendrites have more nodes and hence greater total length. In fact, the total length of each dendrite was the only parameter useful in distinguishing between neurons of the visual and somesthetic areas.

The visual system in the brain refers to both subcortical and neocortical structures. In primates and other animals, the retina projects primarily to the superior colliculus and pretectum of the midbrain and to the lateral geniculate nucleus of the thalamus. The retina distributes different information to each of these structures through the specific projections of different types of ganglion cells. In the retino-geniculate pathway, three ganglion cell types define three parallel functional streams that reach striate cortex, V1. The visual cortex consists of a large number of distinct areas that are defined by various combinations of architectonic, connectional, physiological, topographic, and behavioral criteria. Each cortical area sends projections to a limited subset of areas. The laminar pattern of the origin and termination of these pathways defines feedforward, feedback, and lateral directions between pairs of areas. These laminar features allow the characterization of an anatomical hierarchy of visual areas. Embedded within this hierarchy are several types of functional streams: a dorsal stream that processes ‘where’ objects are and a ventral stream that processes the ‘what’ of objects. At lower levels of the hierarchy, three functional streams arise that are related to color and brightness, form, and motion processing. These three streams are segregated into functional modules within areas V1 and V2 that are then disseminated to higher cortical areas. Human visual cortex can be subdivided into a number of discrete cortical areas on the basis of visual topography and/or architecture. Thus, the human visual cortex contains a number of areas that are very similar to those found in the occipital lobe of macaque monkeys and other non-human primates.

In a recent series of investigations, dramatic differences in pyramidal cell structure have been demonstrated in the primate neocortex. Initial studies in the cortex of the macaque monkey revealed a remarkable degree of heterogeneity in the structure of pyramidal cells sampled from homologous cortical layers among functionally related cortical areas. For example, there was, on average, a 13-fold difference in the number of spines in the dendritic trees of layer III pyramidal cells involved in visual processing. Moreover, the differences in the complexity of pyramidal cell structure among cortical areas were not random: cells involved in what are generally accepted to be more complex aspects of visual processing had more complex structure. Similar systematic trends in pyramidal cell specialization were found among cortical areas involved in somatosensation, locomotion, emotion, and even in executive cortical functions such as conceptualization, planning, and prioritizing. These studies revealed up to a 16-fold difference in the number of dendritic spines (putative excitatory inputs) in the dendritic trees of pyramidal cells in different cortical areas of the adult macaque monkey brain. Moreover, there are systematic and dramatic differences in the branching structure of pyramidal cells in the macaque cerebral cortex, with neurons in executive cortical areas having significantly more branches than those in sensory or motor cortex.

Comparative studies of pyramidal cell structure have revealed some interesting similarities, and some striking differences, in the structure of pyramidal cells in the brains of various primate species. With up to a 30-fold difference in the estimates of the total number of dendritic spines in the dendritic trees of pyramidal cells in the primate cerebral cortex there is considerable scope for receiving different numbers of excitatory inputs. Moreover, the most branched pyramidal cells observed to date are found in the human prefrontal cortex, being, on average, more than twice as branched as those in the galago prefrontal cortex. Thus, species differences in pyramidal cell structure not only influence the number of inputs received within the dendritic tree, but how these inputs are integrated. Here we present an overview of the comparative data obtained from visual, somatosensory, motor, cingulate, and prefrontal cortex of the human, baboon, macaque monkey, vervet monkey, owl monkey, marmoset monkey, and galago. From these data, and those obtained from the archontan tree shrew, one can speculate on the functional consequences of specialization of the pyramidal cell phenotype, and how these may vary between species. New insights into evolutionary and developmental pressures that may shape the pyramidal cell phenotype in the adult brain are presented.

A fundamental and long-standing question in neuroscience is what is special about the neocortex of humans and how does it differ from that of other species. It is generally thought that during evolution, the neocortex expanded in larger brains due to the addition of microcircuits with the same basic structure. Hence, it is considered unlikely that new types of neurons or other fundamental differences exist. Here, we focus on certain features that have been highlighted by comparative microanatomical studies of the neocortex that emphasize the differences between the human neocortex and that of other mammals. The notion of uniformity in the neocortex with respect to the density and the types of neurons found in columns has been recently challenged. We present evidence that the uniformity of cortex has been overstated and that there are actually wide variations in cortical organization. The proportion of GABAergic interneurons is higher in primates than in rats and, moreover, certain subtypes of interneurons are lacking or greatly modified in some species. Together with the distinct synaptology in the neuropil and in the number of synapses per neuron, these differences clearly highlight the variability in the design of microcircuits between cortical areas and species. Given our ignorance regarding many aspects of the organization of the cerebral cortex and the great number of mammalian species whose cortical structure remains unexplored, what we currently conceive as general diagrams of basic neocortical circuits should be considered an oversimplification. Based on our studies and those of a number of other laboratories, we support the idea that the human neocortex shows unique specialization that is likely to be crucial for human cortical function.