Spinogenesis and Pruning from Early Visual Onset to Adulthood: An Intracellular Injection Study of Layer III Pyramidal Cells in the Ventral Visual Cortical Pathway of the Macaque Monkey

Elston, Guy N.; Oga, Tomofumi; Okamoto, Tsuguhisa; Fujita, Ichiro

doi:10.1093/cercor/bhp203

Cited by 36 publications

(78 citation statements)

References 78 publications

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“…In low-expanding visual and auditory cortex (Heschl's gyrus), synaptic density is 50-100% greater and is closer to peak density than the high-expanding middle frontal gyrus (1). The neonatal macaque visual and auditory cortex are close to mature dendritic spine and dendritic field area, whereas the anterior prefrontal and lateral temporal cortex have approximately half the density and field area found in adulthood (23)(24)(25). In newborn humans, the local cerebral metabolic rate for glucose is markedly higher (by 15-25%) in the low-expanding medial temporal and visual cortex than in the high-expanding dorsolateral prefrontal cortex (DLPFC) (26).…”

Section: Discussionmentioning

confidence: 99%

Similar patterns of cortical expansion during human development and evolution

Hill¹,

Inder²,

Neil³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

684

589

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The cerebral cortex of the human infant at term is complexly folded in a similar fashion to adult cortex but has only one third the total surface area. By comparing 12 healthy infants born at term with 12 healthy young adults, we demonstrate that postnatal cortical expansion is strikingly nonuniform: regions of lateral temporal, parietal, and frontal cortex expand nearly twice as much as other regions in the insular and medial occipital cortex. This differential postnatal expansion may reflect regional differences in the maturity of dendritic and synaptic architecture at birth and/or in the complexity of dendritic and synaptic architecture in adults. This expression may also be associated with differential sensitivity of cortical circuits to childhood experience and insults. By comparing human and macaque monkey cerebral cortex, we infer that the pattern of human evolutionary expansion is remarkably similar to the pattern of human postnatal expansion. To account for this correspondence, we hypothesize that it is beneficial for regions of recent evolutionary expansion to remain less mature at birth, perhaps to increase the influence of postnatal experience on the development of these regions or to focus prenatal resources on regions most important for early survival.T he human cerebral cortex is characterized by regional nonuniformities in cellular structure that change with age. Near term, there are regional variations in synaptic density (1, 2), dendritic length, and dendritic spine density (3). Postnatally, synaptic density increases dramatically, reaches a peak density in early childhood, and then undergoes synaptic pruning with a 2-fold or greater reduction (4). The time course of these synaptic changes differs across regions, with primary sensory areas attaining peak density and adult levels earlier than higher order "association" areas (2, 5). In adults, there are large regional nonuniformities in neuronal density (6), dendritic size, branching complexity, and spine density (7).This evidence for cellular nonuniformities provides grounds for anticipating regional differences in macroscopic aspects of postnatal cortical maturation. Indeed, studies of gray matter volume and overall brain growth provide evidence for complex regional patterns of morphological change during childhood and adolescence (8, 9). We recently used a surface-based approach to compare cortical structure in human term infants to adults. That analysis suggested that although many adult cortical shape characteristics are well established at birth, there may be regional differences in the maturity of cortical folding in term infants compared with adults (10).Comparisons with nonhuman primates, especially the intensively studied macaque monkey, provide another basis for evaluating regional differences in cortical maturation. Since the evolutionary divergence between humans and macaques ∼25 million years ago (11), cortical expansion has been far greater in human lineage than in the macaque lineage. Compared with the macaque cortex, the human c...

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Section: Discussionmentioning

confidence: 99%

Similar patterns of cortical expansion during human development and evolution

Hill¹,

Inder²,

Neil³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

684

589

View full text Add to dashboard Cite

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“…Thus, it is tempting to conclude that highly complex pyramidal cells in the dorsolateral gPFC is a characteristic of the latter species, which may differ from that in other primates that diverged earlier, such as New World monkeys and the great apes. Alternatively, the apparent species differences may reflect regional variation in neuronal maturation rates (Jacobs and Scheibel, 1993; Jacobs et al, 1995, 1997; Page et al, 2002; Duan et al, 2003; Elston et al, 2009, 2010a,b) or arise through sampling different subsets of projection neurons in the different cortical areas, which have been shown to differ in both their morphology (Schofield et al, 1987; Hallman et al, 1988; Hübener and Bolz, 1988; de Lima et al, 1990; Hübener et al, 1990; Einstein, 1996; Matsubara et al, 1996; Duan et al, 2002; Soloway et al, 2002; Elston and Rosa, 2006) and density (Jones and Powell, 1970; Barbas, 1992; Young, 1992; Pandya and Yeterian, 2000; Petrides, 2000; Collins et al, 2005) in different cortical areas. In either case, the result is consistent with our main conclusion that pyramidal cells develop differently among cortical areas and mature into specialized circuits.…”

Section: Discussionmentioning

confidence: 99%

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

Elston¹,

Benavides-Piccione

Elston³

et al. 2011

Front. Neuroanat.

108

105

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The most ubiquitous neuron in the cerebral cortex, the pyramidal cell, is characterized by markedly different dendritic structure among different cortical areas. The complex pyramidal cell phenotype in granular prefrontal cortex (gPFC) of higher primates endows specific biophysical properties and patterns of connectivity, which differ from those in other cortical regions. However, within the gPFC, data have been sampled from only a select few cortical areas. The gPFC of species such as human and macaque monkey includes more than 10 cortical areas. It remains unknown as to what degree pyramidal cell structure may vary among these cortical areas. Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates. We found marked heterogeneity in pyramidal cell structure within and between these regions. Moreover, trends for gradients in neuronal complexity varied among species. As the structure of neurons determines their computational abilities, memory storage capacity and connectivity, we propose that these specializations in the pyramidal cell phenotype are an important determinant of species-specific executive cortical functions in primates.

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“…Myelin maps were generated by computing the T1w/T2w ratio for each cortical gray matter voxel, mapping it to individual cortical surfaces, and registering the individuals to a species-specific atlas surface (Glasser and Van Essen 2011) using the MSM registration method myelinated higher cognitive regions, whereas the least expansion (~2-fold) occurs in early sensory areas (Hill et al 2010). A likely cellular-level correlate is that, in the macaque, dendritic arbors sizes and synapse number increase between birth and adulthood in inferotemporal cortex, whereas there is a net decrease in both measures for early visual areas (Elston et al 2010). Thus, in both species regional differences in neuronal density, average dendritic arbor size, and myelin content conform to a general pattern that provides important insights for understanding brain function, evolution, and development.…”

Section: Convolutions and Folding Variabilitymentioning

confidence: 98%

Parcellations and Connectivity Patterns in Human and Macaque Cerebral Cortex

Essen

Donahue

Dierker

et al. 2016

Research and Perspectives in Neurosciences

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To decipher brain function, it is vital to know how the brain is wired. This entails elucidation of brain circuits at multiple scales, including microscopic, mesoscopic, and macroscopic levels. Here, we review recent progress in mapping the macroscopic brain circuits and functional organization of the cerebral cortex in primates-humans and macaque monkeys, in particular. There are many similarities across species in terms of overall patterns of cortical gray matter myelination as well as functional areas that are presumed to be homologous. However, there are also many important species differences, including cortical convolutions that are much more complex and more variable in humans than in monkeys. Our ability to analyze structure and function has benefited from improved methods for intersubject registration that cope with this individual variability. To characterize long-distance connectivity, powerful but indirect methods are now available, including resting-state functional connectivity and diffusion imaging coupled with probabilistic tractography. We illustrate how connectivity inferred from diffusion imaging and tractography can be evaluated in relation to 'ground truth' based on anatomical tracers in the macaque. Interspecies registration between human and macaque cortex based on presumed interspecies homologies demonstrates an impressive degree of areal expansion in regions associated with higher cognitive function.

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Spinogenesis and Pruning from Early Visual Onset to Adulthood: An Intracellular Injection Study of Layer III Pyramidal Cells in the Ventral Visual Cortical Pathway of the Macaque Monkey

Cited by 36 publications

References 78 publications

Similar patterns of cortical expansion during human development and evolution

Similar patterns of cortical expansion during human development and evolution

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

Parcellations and Connectivity Patterns in Human and Macaque Cerebral Cortex

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