Christine E. Collins

Cellular scaling rules for primate brains

Primates are usually found to have richer behavioral repertoires and better cognitive abilities than rodents of similar brain size. This finding raises the possibility that primate brains differ from rodent brains in their cellular composition. Here we examine the cellular scaling rules for primate brains and show that brain size increases approximately isometrically as a function of cell numbers, such that an 11× larger brain is built with 10× more neurons and ≈12× more nonneuronal cells of relatively constant average size. This isometric function is in contrast to rodent brains, which increase faster in size than in numbers of neurons. As a consequence of the linear cellular scaling rules, primate brains have a larger number of neurons than rodent brains of similar size, presumably endowing them with greater computational power and cognitive abilities.

Neuron densities vary across and within cortical areas in primates

The numbers and proportion of neurons in areas and regions of cortex were determined for a single cortical hemisphere from two prosimian galagos, one New World owl monkey, one Old World macaque monkey, and one baboon. The results suggest that there is a common plan of cortical organization across the species examined here and also differences that suggest greater specializations in the Old World monkeys. In all primates examined, primary visual cortex (V1) was the most neuron-dense cortical area and the secondary visual areas had higher-than-average densities. Primary auditory and somatosensory areas tended to have high densities in the Old World macaque and baboon. Neuronal density varies less across cortical areas in prosimian galagos than in the Old World monkeys. Thus, cortical architecture varies greatly within and across primate species, but cell density is greater in cortex devoted to the early stages of sensory processing.

The basic nonuniformity of the cerebral cortex

Evolutionary changes in the size of the cerebral cortex, a columnar structure, often occur through the addition or subtraction of columnar modules with the same number of neurons underneath a unit area of cortical surface. This view is based on the work of Rockel et al. [Rockel AJ, Hiorns RW, Powell TP (1980) The basic uniformity in structure of the neocortex. Brain 103:221–244], who found a steady number of approximately 110 neurons underneath a surface area of 750 μm2 (147,000 underneath 1 mm2) of the cerebral cortex of five species from different mammalian orders. These results have since been either corroborated or disputed by different groups. Here, we show that the number of neurons underneath 1 mm2 of the cerebral cortical surface of nine primate species and the closely related Tupaia sp. is not constant and varies by three times across species. We found that cortical thickness is not inversely proportional to neuronal density across species and that total cortical surface area increases more slowly than, rather than linearly with, the number of neurons underneath it. The number of neurons beneath a unit area of cortical surface varies linearly with neuronal density, a parameter that is neither related to cortical size nor total number of neurons. Our finding of a variable number of neurons underneath a unit area of the cerebral cortex across primate species indicates that models of cortical organization cannot assume that cortical columns in different primates consist of invariant numbers of neurons.

The Primate visual system

Introduction: A Brief Overview of the Primate Visual System. The K, P, and M Pathways from Retina to Cortex. The Pulvinar Complex. The Development of Neuron Response Properties in Primary Visual Cortex. The Second Visual Area, V2. The Superior Colliculus. Early Visual Areas: V2, V3, DM, DL, and MT. Plasticity of Visual Cortex in Adults. Processing Hierarchies in Visual Cortex. Visuomotor Areas in Frontal and Parietal Cortex. Specializations of Human Visual Cortex. Maps of the Visual Field in the Cerebral Cortex of Primates: Functional Organization and Significance. Face Expertise and Category Specialization in the Human Occipitotemporal Cortex. Motion Processing in Human Visual Cortex. The Functional Organization of Monkey Inferotemporal Cortex. Comparative Studies of Pyramidal Neurons in Visual Cortex of Monkeys. Feedback Connections: Splitting the Arrow.

Large-Scale Reorganization in the Somatosensory Cortex and Thalamus after Sensory Loss in Macaque Monkeys

Adult brains undergo large-scale plastic changes after peripheral and central injuries. Although it has been shown that both the cortical and thalamic representations can reorganize, uncertainties exist regarding the extent, nature, and time course of changes at each level. We have determined how cortical representations in the somatosensory area 3b and the ventroposterior (VP) nucleus of thalamus are affected by long standing unilateral dorsal column lesions at cervical levels in macaque monkeys. In monkeys with recovery periods of 22–23 months, the intact face inputs expanded into the deafferented hand region of area 3b after complete or partial lesions of the dorsal columns. The expansion of the face region could extend all the way medially into the leg and foot representations. In the same monkeys, similar expansions of the face representation take place in the VP nucleus of the thalamus, indicating that both these processing levels undergo similar reorganizations. The receptive fields of the expanded representations were similar in somatosensory cortex and thalamus. In two monkeys, we determined the extent of the brain reorganization immediately after dorsal column lesions. In these monkeys, the deafferented regions of area 3b and the VP nucleus became unresponsive to the peripheral touch immediately after the lesion. No reorganization was seen in the cortex or the VP nucleus. A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.

The organization of sensory cortex

Recent studies of primary visual cortex (V1) redefine layers 3 and 4 of V1 in monkeys and show that monkeys, apes and humans have different laminar specializations. Projections from V1 define a smaller, but complete, third visual area, and a dorsomedial area. The middle temporal visual area has two types of motion-sensitive modules with inputs from cytochrome oxidase columns in V1. Second-level somatosensory areas have been described in humans, and a second-level auditory area is shown to respond to somatosensory stimuli.

Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch)

The organization of anterior and lateral somatosensory cortex was investigated in titi monkeys (Callicebus moloch). Multiunit microelectrode recordings were used to identify multiple representations of the body, and anatomical tracer injections were used to reveal connections. (1) Representations of the face were identified in areas 3a, 3b, 1, S2, and the parietal ventral area (PV). In area 3b, the face was represented from chin/lower lip to upper lip and neck/upper face in a rostrocaudal sequence. The representation of the face in area 1 mirrored that of area 3b. Another face representation was located in area 3a. Adjoining face representations in S2 and PV exhibited mirror‐image patterns to those of areas 3b and 1. (2) Two representations of the body, the rostral and caudal ventral somatosensory areas (VSr and VSc), were found in the dorsal part of the insula. VSc was roughly a reversal image of the S2 body representation, and VSr was roughly a reversal of PV. (3) Neurons in the insula next to VSr and VSc responded to auditory stimuli or to both auditory and somatosensory stimuli. (4) Injections of tracers within the hand representations in areas 3b, 1, and S2 revealed reciprocal connections between these three areas. Injections in areas 3b and 1 labeled the ventroposterior nucleus, whereas injections in S2 labeled the inferior ventroposterior nucleus. The present study demonstrates features of somatosensory cortex of other monkeys in titi monkeys, while revealing additional features that likely apply to other primates. J. Comp. Neurol. 476:363–387, 2004.

Cellular Scaling Rules for the Brains of an Extended Number of Primate Species

What are the rules relating the size of the brain and its structures to the number of cells that compose them and their average sizes? We have shown previously that the cerebral cortex, cerebellum and the remaining brain structures increase in size as a linear function of their numbers of neurons and non-neuronal cells across 6 species of primates. Here we describe that the cellular composition of the same brain structures of 5 other primate species, as well as humans, conform to the scaling rules identified previously, and that the updated power functions for the extended sample are similar to those determined earlier. Accounting for phylogenetic relatedness in the combined dataset does not affect the scaling slopes that apply to the cerebral cortex and cerebellum, but alters the slope for the remaining brain structures to a value that is similar to that observed in rodents, which raises the possibility that the neuronal scaling rules for these structures are shared among rodents and primates. The conformity of the new set of primate species to the previous rules strongly suggests that the cellular scaling rules we have identified apply to primates in general, including humans, and not only to particular subgroups of primate species. In contrast, the allometric rules relating body and brain size are highly sensitive to the particular species sampled, suggesting that brain size is neither determined by body size nor together with it, but is rather only loosely correlated with body size.

A rapid and reliable method of counting neurons and other cells in brain tissue: a comparison of flow cytometry and manual counting methods

It is of critical importance to understand the numbers and distributions of neurons and non-neurons in the cerebral cortex because cell numbers are reduced with normal aging and by diseases of the CNS. The isotropic fractionator method provides a faster way of estimating numbers of total cells and neurons in whole brains and dissected brain parts. Several comparative studies have illustrated the accuracy and utility of the isotropic fractionator method, yet it is a relatively new methodology, and there is opportunity to adjust procedures to optimize its efficiency and minimize error. In the present study, we use 142 samples from a dissected baboon cortical hemisphere to evaluate if isotropic fractionator counts using a Neubauer counting chamber and fluorescence microscopy could be accurately reproduced using flow cytometry methods. We find greater repeatability in flow cytometry counts, and no evidence of constant or proportional bias when comparing microscopy to flow cytometry counts. We conclude that cell number estimation using a flow cytometer is more efficient and more precise than comparable counts using a Neubauer chamber on a fluorescence microscope. This method for higher throughput, precise estimation of cell numbers has the potential to rapidly advance research in post-mortem human brains and vastly improve our understanding of cortical and subcortical structures in normal, injured, aged, and diseased brains.

Topographic patterns of v2 cortical connections in a prosimian primate (Galago garnetti)

Topographic patterns of cortical connections of the second visual area (V2) were examined in a lorisiform prosimian primate (Galago garnetti). Up to five different tracers were injected into dorsal and ventral V2. Tracers included wheat germ agglutinin conjugated to horseradish peroxidase (WGA‐HRP) and up to four fluorochromes. Tracer injections consistently labeled neurons and terminals in primary visual cortex (V1), V2, the middle temporal area (MT), and the dorsolateral visual area (DL). Labeled neurons were also found in other proposed extrastriate areas such as the dorsomedial visual area (DM), dorsointermediate area (DI), middle temporal crescent (MTc), medial superior temporal area (MST), ventral posterior parietal area (VPP), and caudal inferotemporal cortex (ITc), but these connections were more variable and less dependent on the retinotopic position of injection sites in V2. Areal boundaries were identified by differences in cytochrome oxidase (CO) and myelin staining. We conclude that V2 cortical connections in prosimian galagos are similar to those in simian primates, suggesting that prosimians and other lines of primate evolution have retained several visual areas from a common ancestor that relate to V2 in similar ways. Architectural features of striate and extrastriate areas in prosimian galagos are similar to simian primates, with notable exceptions such as stripes in V2, which appear to be less differentiated in galagos. J. Comp. Neurol. 431:155–167, 2001.