Aging in the rat olfactory system: Correlation of changes in the olfactory epithelium and olfactory bulb

Hinds, James W.; McNelly, Nancy A.

doi:10.1002/cne.902030308

Cited by 167 publications

(104 citation statements)

References 22 publications

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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: 71%

“…The significant loss of glomerular A:D synapses we report here is likely related to global reductions in OSN density and OR-specific OSN subpopulations (4,14,(18)(19)(20). In contrast, D:D synapses are also lost despite stability of the number of PG and mitral/tufted cells.…”

Section: Discussionmentioning

confidence: 62%

“…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.…”

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confidence: 99%

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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: 71%

Section: Discussionmentioning

confidence: 62%

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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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“…Anatomical changes associated with aging have been detected in both peripheral olfactory structures, e.g., olfactory epithelium (Naessen, 1971;Dodson and Bannister, 1980), and central olfactory pathways, e.g., olfactory bulb (Liss and Gomez, 1958;Hinds and McNelly, 1981), but their relative contributions to the age-related functional deficits are unknown.…”

Section: Introductionmentioning

confidence: 99%

Olfactory event-related potentials in normal human subjects: effects of age and gender

Evans

Starr

1995

Electroencephalography and Clinical Neurophysiology

116

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Olfactory event-related potentials in normal human subjects: effects of age and gender AbstractBehavioral and electrophysiological testing of olfactory function was performed in 33 normal human male and female subjects, 18-83 years of age. Acuity for odor identification and odor detection was verified by standard psychophysical tests. For evoked potential testing, a constant flow olfactometer provided odorant stimuli (amyl acetate) or air control stimuli that were presented to the right nostril by a nasal cannula at a flow rate of 5 1/min, duration of 40 msec and random interstimulus intervals of 6-30 sec. The behavioral tests revealed no significant difference between males and females, whereas increasing age was associated with a decline in performance on the odor identification test. No reproducible evoked potentials were recorded in response to the air control stimulus. Potentials to the odorant stimulus consisted of 4 components named P1, N1, P2 and N2. A significant correlation was found between P2 latency and odor identification test scores, suggesting a relationship between the generation of the P2 component and olfactory processing. P2 peak latency increased significantly with age at 2.5 msec/year. An age-related decline in N1-P2 interpeak amplitude was seen in male subjects. Topographic differences were seen in the P2 peak amplitude and the N1-P2 and P2-N2 interpeak amplitudes such that their amplitudes were greatest at Cz and Pz. On average, N1-P2 interpeak amplitudes were larger in the female subjects than in the male subjects, possibly revealing a hormonal influence on the olfactory event-related potential.

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“…The present study also demonstrated difference in the shape of dendrites extending from perikarya located at various heights of the epithelium. The following reasons are possible explanations for this phenomenon: 1) Olfactory receptor cells are known to be continuously renewed [8,29]. Since newly differentiated cells have to extend their dendrite to the surface of epithelium through a densely packed cell mass, the extension of dendrite may be mechanically affected, resulting in thin and winding dendrites.…”

Section: Morphology Of Olfactory Receptor Cells: the Detailedmentioning

confidence: 99%

Morphological Analysis of Olfactory Receptor Cells Using Whole-Mount Preparations of the Rat Nasal Mucosa.

Hosaka

Yanase

Iwanaga

1998

The Journal of Veterinary Medical Science

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ABSTRACT. The distribution and entire shape of olfactory receptor cells were investigated by means of whole-mount preparations of the nasal mucosa. Whole mucosa isolated from the nasal septum of rats was processed, as "a free-floating section", and examined by the avidin-biotin complex (ABC) method using antisera against protein gene product 9.5 (PGP 9.5) and calbindin. Essentially all receptor cells were immunolabeled with the PGP 9.5 antiserum, but only half of PGP 9.5-immunoreactive cells were calbindin-immunoreactive. In the immunostaining of whole-mount preparations, pretreatment of tissues by freeze-thawing and dipping in ethanol and xylene greatly improved the permeability of antibodies. Overview of the nasal septum showed that the dorsal and ventral portions of the rostral olfactory area extended deeply into the respiratory area, making a "semi-lunar" shape. The boundary between the two areas was clearly demarcated, although several receptor cells were scattered in the respiratory area near the boundary. Observation at higher magnification clearly demonstrated that several axons derived from perikarya gathered to form nerve bundles showing a dendritic pattern. Proximal axons close to perikarya displayed beaded structures with intense immunoreactivity. They were electron-microscopically identified as swollen portions of axons which might be formed in association with the axonal flow. The present study showed that whole-mount preparation of the nasal mucosa for immunohistochemistry is a useful tool to analyze the morphology of olfactory receptor cells and axons. -KEY WORDS: calbindin, immunohistochemistry, olfactory receptor cell, PGP 9.5, whole-mount preparation.J. Vet. Med. Sci. 60(8): 897-904, 1998 been done mainly by using thin tissue sections. Even if we can specifically immunolabel the receptor cells, it is difficult to visualize their distribution and morphology throughout the nasal mucosa. Whole-mount preparation has the advantage of making it possible to observe wide areas and the entire shape of a structure, even three-dimensionally. Its usefulness has been shown in observation of nerve fibers and lymphatic vessels distributed in membranous tissues such as the iris, urethra, intestine and tracheal mucosa [4,21,22,26]. In the present study, immunohistochemical staining using PGP 9.5 and calbindin antisera was applied to whole-mount preparations of the nasal mucosa to demonstrate the detailed distribution and entire shape of olfactory receptor cells including the dendrite and axon. Furthermore, electron microscopic observation revealed the nature of beaded structures found on proximal axons of receptor cells. MATERIALS AND METHODSImmunohistochemistry: Thirty-four male Wistar rats, weighing 200-300 g, were used in this study. The animals were deeply anesthetized with an intraperitoneal injection of pentobarbital sodium (50 ml/kg body weight) and perfused through the ascending aorta with physiological saline and subsequently with 4% paraformaldehyde in 0.1 M phosphate buffer, pH 7.4. The nasal sep...

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Aging in the rat olfactory system: Correlation of changes in the olfactory epithelium and olfactory bulb

Cited by 167 publications

References 22 publications

Age-induced disruption of selective olfactory bulb synaptic circuits

Age-induced disruption of selective olfactory bulb synaptic circuits

Olfactory event-related potentials in normal human subjects: effects of age and gender

Morphological Analysis of Olfactory Receptor Cells Using Whole-Mount Preparations of the Rat Nasal Mucosa.

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