Aging of the rat olfactory bulb: Growth and atrophy of constituent layers and changes in size and number of mitral cells

Hinds, James W.; McNelly, Nancy A.

doi:10.1002/cne.901710304

Cited by 233 publications

(92 citation statements)

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“…Contrary to earlier reports of extensive volume and cell losses in the aging brain, our data suggest more subtle region-and layer-specific changes (1, 2). In the OB, there are reports of both strain-and species-dependent effects of aging (14)(15)(16)(17). Our results, which included more intermediate time points, establish that OB volume is stable from 2 mo onward in C57BL/6J mice.…”

Section: Discussionsupporting

confidence: 70%

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Age-induced disruption of selective olfactory bulb synaptic circuits

Richard

Taylor²,

Greer³

2010

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

120

125

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Little is known about how normal aging affects the brain. Recent evidence suggests that neuronal loss is not ubiquitous in aging neocortex. Instead, subtle and still controversial, region-and layerspecific alterations of neuron morphology and synapses are reported during aging, leading to the notion that discrete changes in neural circuitry may underlie age-related cognitive deficits. Although deficits in sensory function suggest that primary sensory cortices are affected by aging, our understanding of the age-related cellular and molecular changes is sparse. To assess the effect of aging on the organization of olfactory bulb (OB) circuitry, we carried out quantitative morphometric analyses in the mouse OB at 2, 6, 12, 18, and 24 mo. Our data establish that the volumes of the major OB layers do not change during aging. Parallel to this, we are unique in demonstrating that the stereotypic glomerular convergence of M72-GFP OSN axons in the OB is preserved during aging. We then provide unique evidence of the stability of projection neurons and interneurons subpopulations in the aging mouse OB, arguing against the notion of an age-dependent widespread loss of neurons. Finally, we show ultrastructurally a significant layer-specific loss of synapses; synaptic density is reduced in the glomerular layer but not the external plexiform layer, leading to an imbalance in OB circuitry. These results suggest that reduction of afferent synaptic input and local modulatory circuit synapses in OB glomeruli may contribute to specific age-related alterations of the olfactory function.aging | axodendritic synapses | dendrodendritic synapses | mitral cells A ge-related neurodegenerative diseases, such as Parkinson and Alzheimer's, involve localized or widespread neuronal loss, but little is known about the changes occurring in the brain during normal aging. A growing consensus argues against widespread neuronal loss and atrophy during aging (1, 2). Rather, subtle region-and layer-specific alterations of neuronal morphology and synaptic connections are reported in the neocortex and hippocampus, where they may contribute to age-related cognitive deficits.The laminar organization of olfactory bulb (OB) neurons and synapses provides a simplified cortical model in which we can probe principles of neuronal and synaptic organization during aging. Sensory functions are affected by aging, including alterations in olfactory acuity, discrimination, and memory (3-12). The OB is the first central relay in the pathway processing odor information: it receives afferent input from olfactory sensory neurons (OSNs) located in the olfactory epithelium (OE) and is responsible for detecting odors in the nasal cavity. OSN axons synapse on mitral/tufted cell dendrites in OB glomerular neuropils. OB local interneurons modulate the activity of mitral/tufted cells, contributing to odor signal integration, before propagation to the piriform cortex. Projections from the OE to the OB are organized in an odor receptor (OR) map; each subpopulation of OSNs expressin...

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Section: Discussionsupporting

confidence: 70%

“…Some agerelated changes in the OE and OB were reported, mainly in rats (4,(14)(15)(16)(17)(18)(19)(20), but none document the kinetics of the defects. Here, we report quantitative morphometric analyses of the aging mouse OB at 2, 6, 12, 18, and 24 mo, focusing on changes in layer morphology, neuronal populations, synaptic circuitry, and OR map.…”

mentioning

confidence: 99%

Age-induced disruption of selective olfactory bulb synaptic circuits

Richard

Taylor²,

Greer³

2010

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

120

125

View full text Add to dashboard Cite

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“…From four to eighteen months of age, sexually mature albino mice have significant decreases in VRN nuclear density and total VRN numbers per VNO (Wilson & Raisman, 1980). Age-related reduction is also well documented for structures of the main olfactory system in humans (Bhatnagar et al, 1987;Meisami et al, 1998) and mice (Hinds & McNelly, 1977). More notably, a recent study on captive mouse lemurs (Microcebus murinus), revealed an age-related decline in the olfactory abilities as well as endocrine responses of males to female urine (Aujard & Nemoz-Bertholet, 2004), a phenomenon for which VNNE deficits may also play a role.…”

Section: Discussionmentioning

confidence: 84%

The vomeronasal organ of greater bushbabies (Otolemur spp.): Species, sex, and age differences

et al. 2005

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The present study examined interspecies, intersexual, and age-related changes in size of the vomeronasal neuroepithelium (VNNE) of two species of greater bushbabies (genus Otolemur, Infraorder Lorisiformes, Suborder Strepsirrhini). Tissue blocks containing the vomeronasal organs of nine O. crassicaudatus (8 adults, 1 neonate) and ten O. garnettii (9 adults, 1 neonate) were studied by means of serial paraffin sectioning and computer-based reconstruction of VNNE volume. In addition, the immunoreactivity of the VNNE to two neuronal markers, neuron-specific beta tubulin (BT) and olfactory marker protein (OMP) was compared between species, sexes, and ages. Results indicated that a clear VNNE is present at birth in both species, and OMP immunoreactivity was verified in O. garnettii at birth. Male and female adults of both species showed OMP-immunoreactive and BT-immunoreactive neurons in the VNNE. Immunohistochemical findings indicated that all males and the youngest females had the thickest VNNE, especially at the marginal junctions with the receptor-free epithelium. Results of a 2-way Analysis of Variance (ANOVA, species x sex) revealed no significant differences in VNNE length or volume between species, but O. crassicaudatus had significantly ( p < 0.05) greater palatal length. Significant ( p < 0.05) differences also were found between sexes in VNNE volume, but no significant differences in palatal length or VNNE length. The distribution of VNNE volume against age indicated that the sex differences were more pronounced in O. crassicaudatus than O. garnettii. For both species and sexes, distribution of VNNE volume against age suggested an age-related reduction in volume. These findings demonstrate postnatal plasticity in VNNE size in Otolemur that is reminiscent of that found for olfactory structures in some rodents. Bushbabies or other strepsirrhine primates may offer an opportunity for further understanding of behavioral correlates of VNNE postnatal plasticity, which may represent primitive functional characteristics of the order Primates.Abbreviation: BT, beta tubulin; IHC, immunohistochemistry; OMP, olfactory marker protein; RFE, receptor-free epithelium; VNNE, vomeronasal neuroepithelium; VNO, vomeronasal organ; VRN, vomeronasal receptor neurons.

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“…Thus the somatic hypertrophy observed in this study from the 24th month onward could be explained as a compensatory mechanism to maintain the same total somatic volume in spite of the increase in the total volume in the dLGN. This, according to Hinds and McNelly (1977), Flood et al, (1985), and Coleman and Flood (1986), could be related to an increase in the dendritic tree in order to maintain the existing synaptic connections, despite the increase in the dLGN total volume, or perhaps, to compensate for the decrease in the number of synapses and/or in their efficiency during aging (Ahmad and Spear, 1993).…”

Section: Discussionmentioning

confidence: 99%

Quantitative morphological changes in neurons from the dorsal lateral geniculate nucleus of young and old rats

et al. 1997

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Background: We studied the morphological changes occurring in neurons from the dorsal lateral geniculate nucleus (dLGN) during aging by analysing the size and shape of cell bodies and nuclei.Methods: Male albino Wistar rats, aged 3, 18, 24, and 30 months, were used. After appropriate tissue preparation and following the usual histological procedure, the profiles of 1,920 neuronal bodies and nuclei were drawn using a camera lucida. Data was later recorded and processed with a semiautomatic image analyser.Results and conclusions: We observed that dLGN neurons do not change in size from the age of 3-24 months. Between 24 and 30 months, the soma and nucleus of the cell undergo hypertrophy, 32.8% and 35.6%, respectively, when compared to those from 3-month-old animals (P F 0.01). Furthermore, we found a high correlation between cell body size/nucleus size, which does not disappear with age. The r values (correlation coefficient) were 0.7998, 0.8662, 0.8433 and 0.7304, and R 2 (determination coefficient) was equal to 0.6397, 0.7504, 0.7112, and 0.5335. These latter values show that in 63.97%, 75.04%, 71.12%, and 53.35% of cases, respectively, modifications in somata size were accompanied by similar changes in nucleus size, and vice-versa. The study of the shape of the soma and nucleus of the cell revealed that both structures have a rounded-oval configuration that does not change in a significant way from adulthood to old age. Anat.

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Aging of the rat olfactory bulb: Growth and atrophy of constituent layers and changes in size and number of mitral cells

Cited by 233 publications

References 50 publications

Age-induced disruption of selective olfactory bulb synaptic circuits

Age-induced disruption of selective olfactory bulb synaptic circuits

The vomeronasal organ of greater bushbabies (Otolemur spp.): Species, sex, and age differences

Quantitative morphological changes in neurons from the dorsal lateral geniculate nucleus of young and old rats

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