Spinogenesis and Pruning Scales across Functional Hierarchies

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

doi:10.1523/jneurosci.5216-08.2009

Cited by 138 publications

(175 citation statements)

References 22 publications

(27 reference statements)

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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%

See 1 more Smart Citation

Similar patterns of cortical expansion during human development and evolution

Hill¹,

Inder²,

Neil³

et al. 2010

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

660

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%

“…Selected regions of interest were mapped to macaque surface atlas (Fig. 5) according to the following study references: V1, MT, Tea (58); V2, LIP, MT 7a (59); FEF (28); TEpd, PFC (23).…”

Section: Methodsmentioning

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.

660

589

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“…Specifically, it has been shown that pyramidal neurons of the prefrontal cortex are characterized by more elaborate dendritic trees than other cortical areas, to support increased connectivity from integrating diverse corticocortical inputs and to orchestrate cognitively complex behaviors (20,31,32,40). Although dendritic arbors are more extensive in the prefrontal cortex relative to other cortical regions in adult humans (31), chimpanzees (32), and macaques (20), the timing of development of these neuronal specializations appears to be species-specific (13,14).…”

Section: Discussionmentioning

confidence: 99%

“…Whereas synaptogenesis occurs synchronously across the entire cerebral cortex in macaques (9), it appears delayed in the prefrontal region in humans (11). In macaques, moreover, densities of spines located on the dendrites of prefrontal pyramidal neurons are higher than other areas from the time of birth and throughout postnatal development (13). In humans, however, dendritic arbors of prefrontal cortex pyramidal neurons reach adult-like morphological complexity and spine density later in development than dendritic arbors in sensory and motor cortices (14).…”

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confidence: 99%

Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans

Bianchi

Stimpson

Duka

et al. 2013

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

121

114

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Neocortical development in humans is characterized by an extended period of synaptic proliferation that peaks in mid-childhood, with subsequent pruning through early adulthood, as well as relatively delayed maturation of neuronal arborization in the prefrontal cortex compared with sensorimotor areas. In macaque monkeys, cortical synaptogenesis peaks during early infancy and developmental changes in synapse density and dendritic spines occur synchronously across cortical regions. Thus, relatively prolonged synapse and neuronal maturation in humans might contribute to enhancement of social learning during development and transmission of cultural practices, including language. However, because macaques, which share a last common ancestor with humans ∼25 million years ago, have served as the predominant comparative primate model in neurodevelopmental research, the paucity of data from more closely related great apes leaves unresolved when these evolutionary changes in the timing of cortical development became established in the human lineage. To address this question, we used immunohistochemistry, electron microscopy, and Golgi staining to characterize synaptic density and dendritic morphology of pyramidal neurons in primary somatosensory (area 3b), primary motor (area 4), prestriate visual (area 18), and prefrontal (area 10) cortices of developing chimpanzees (Pan troglodytes). We found that synaptogenesis occurs synchronously across cortical areas, with a peak of synapse density during the juvenile period (3-5 y). Moreover, similar to findings in humans, dendrites of prefrontal pyramidal neurons developed later than sensorimotor areas. These results suggest that evolutionary changes to neocortical development promoting greater neuronal plasticity early in postnatal life preceded the divergence of the human and chimpanzee lineages.evolution | Golgi stain | brain | ontogeny

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“…After the initial development in the mammalian brain, synapse elimination and refinement occur though interaction with the environment via sensory inputs (Huttenlocher et al, 1982;Elston et al, 2009). However, the detailed mechanisms of this elimination and refinement remain unclear.…”

Section: Relationship Between Synaptic Densities and Network Electricmentioning

confidence: 99%

Measurement of saturation processes in glutamatergic and GABAergic synapse densities during long-term development of cultured rat cortical networks

2013

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The aim of this study was to clarify the saturation processes of excitatory and inhibitory synapse densities during the long-term development of cultured neuronal networks. For this purpose, we performed a long-term culture of rat cortical cells for 35 days in vitro (DIV). During this culture period, we labeled glutamatergic and GABAergic synapses separately using antibodies against vesicular glutamate transporter 1 (VGluT1) and vesicular transporter of -aminobutyric acid (VGAT). The densities and distributions of both types of synaptic terminals were measured simultaneously. Observations and subsequent measurements of immunofluorescence demonstrated that the densities of both types of antibody-labeled terminals increased gradually from 7 to 21-28 DIV. The densities did not show a further increase at 35 DIV and tended to become saturated.Triple staining with VGluT1, VGAT, and microtubule-associated protein 2 (MAP2) enabled analysis of the distribution of both types of synapses, and revealed that the densities of the two types of synaptic terminals on somata were not significantly different, but that glutamatergic synapses predominated on the dendrites during long-term culture.However, some neurons did not fall within this distribution, suggesting differences in synapse distribution on target neurons. The electrical activity also showed an initial increase and subsequent saturation of the firing rate and synchronized burst rate during long-term culture, and the number of days of culture to saturation from the initial increase followed the same pattern under this culture condition.

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Spinogenesis and Pruning Scales across Functional Hierarchies

Cited by 138 publications

References 22 publications

Similar patterns of cortical expansion during human development and evolution

Similar patterns of cortical expansion during human development and evolution

Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans

Measurement of saturation processes in glutamatergic and GABAergic synapse densities during long-term development of cultured rat cortical networks

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