Unilateral odor deprivation: Differential effects due to time of treatment

doi:10.1016/0361-9230(83)90121-1

Brain Research Bulletin

Volume 11, Issue 5, November 1983, Pages 501-503

https://doi.org/10.1016/0361-9230(83)90121-1 Get rights and content

Abstract

Rats were unilaterally deprived of odor stimulation by surgically sealing one naris 1, 30 or 60 days after birth. Thirty days later the laminar volumes of the olfactory bulb ipsilateral to the occluded naris were compared with those ipsilateral to the normal side. Deprivation from days 1–30 resulted in approximately 25% reductions in “deprived” bulb size, corroborating results reported by others. Altered experience at older ages had little effect on laminar volume suggesting that deprivation does not produce atrophy per se, but interacts with early developmental processes to result in differential bulb size.

References (22)

P.C. Brunjes
A versatile and inexpensive planimeter system
J Neurosci Methods
(1983)
P.C. Brunjes
Olfactory bulb maturation in Acomys cahirinus: Is neural growth similar in precocial and altricial murids?
Dev Brain Res
(1983)
P.C. Brunjes et al.
Olfactory granule cell development in normal and hyperthyroid rats
Dev Brain Res
(1982)
E. Meisami
Effects of olfactory deprivation on postnatal growth of the rat olfactory bulb utilizing a new method for production of neonatal unilateral anosmia
Brain Res
(1976)
E. Meisami et al.
A quantitative study of the effects of early unilateral olfactory deprivation on the number and distribution of mitral and tufted cells and the glomeruli in the rat olfactory bulb
Brain Res
(1981)
T.E. Benson et al.
Sensory deprivation affects the developing olfactory system of mice
Soc Neurosci Abstr
(1980)
T.E. Benson et al.
Sensory deprivation affects mitral cell synapses but not size or number
Soc Neurosci Abstr
(1981)
T.E. Benson et al.
Effects of sensory deprivation on the development and maintenance of the olfactory system in mice
Soc Neurosci Abstr
(1978)
G. Gottleib
The role of experience in the development of behavior and the nervous system
P.P.C. Graziadei et al.
Continuous nerve cell renewal in the olfactory system

J.W. Hinds

Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia

J Comp Neurol

(1968)

Cited by (48)

Odorant modulation of neuronal activity and local field potential in sensory-deprived olfactory bulb
2009, Neuroscience
Citation Excerpt :
Anatomical and functional changes in the OB are induced by olfactory sensory deprivation. Anatomically, there is a reduction in size of the OB (Brunjes and Borror, 1983; Brunjes, 1985) primarily due to a decrease in the number of OB granule cells. Functionally, deprivation increases the responsiveness and decreases the specificity of MT cells to odorant stimulation (Guthrie et al., 1990; Wilson and Wood, 1992).
Neuronal discharge and local field potential (LFP) oscillations in the olfactory bulb (OB) are modulated by odorant stimulation. The LFP oscillations have been proposed as the mechanism that facilitates synchronization of OB output neurons and the representation of similar odorants. Gamma LFP oscillations depend on the OB inhibitory network and early sensory deprivation modifies this inhibitory network. However, little is known about the LFP oscillations and neuronal discharge in the deprived OB. We examined the mitral/tufted (MT) cells' oscillatory activity and LFP oscillations in both sensory-deprived and normal OBs in urethane anesthetized rats. We found that MT cells in deprived and normal OBs have similar basal mean firing rate; 44% of the recorded cells in deprived OB and only 8% of the cells in normal OB showed firing rate modulation by odorants, both exhibiting a similar ratio of excitatory to inhibitory responses. A fraction of MT cells exhibited oscillatory discharge centered on gamma (60–70 Hz) and beta (20 Hz) frequencies, although this feature was not consistently dependent on odorant stimulation. Odorants decreased the LFP oscillatory power in the gamma band (35–90 Hz) and increased the power in the beta band (12–30 Hz). The modulation of LFP oscillations by odorants was also predominant in the deprived (53%) compared to the normal OB (17%). In contrast, a higher fraction of MT cells' discharge was locked to the gamma LFP cycle in the normal OB. These results suggest that early unilateral olfactory deprivation increases the OB sensitivity to odorants and reduce the temporal synchrony between unitary activity and gamma LFP oscillations without altering the basal neuronal discharge.
Afferent regulation of neuron number in the cochlear nucleus: Cellular and molecular analyses of a critical period
2006, Hearing Research
The neurons of the cochlear nucleus are dependent on input from the auditory nerve for survival during a critical period of development in a variety of vertebrate species. The molecules that underlie this age-dependent vulnerability to deafferentation are for the most part unknown, although recent studies have begun to yield interesting candidate genes. Here, we review the studies that originally described the presence of afferent dependent neuron survival in the cochlear nucleus and the age-dependency of this effect, as well as more recent work that seeks to understand the mechanisms underlying the neuron loss that occurs and the basis of this critical period. While much of the past work on cochlear nucleus neuronal susceptibility has been conducted looking at one or two genes at a time, recent advances in genomics make it possible to screen tens of thousands of genes while looking for candidate genes that are determinants of the critical period response to afferent deprivation.
Trans-neuronal regulation of cortical apoptosis in the adult rat olfactory system
2003, Brain Research
Citation Excerpt :
Deprivation-induced apoptosis could be due to a variety of mechanisms. For example, although the consequences of adult onset deprivation are relatively minor compared to early onset deprivation in the bulb (e.g., Refs. [4,6,40]), naris occlusion in adult rats produces a variety of changes in the olfactory bulb, including modified temporal patterns of mitral/tufted cell activity [34]. Since olfactory bulb mitral/tufted cells are the primary afferent of the piriform cortex, the enhanced cortical apoptosis may largely be secondary to these bulb changes.
Previous work has identified a population of neurons within the anterior piriform cortex that undergo rapid apoptosis following de-afferentation by olfactory bulbectomy in adult rats. The specific initiation signal for apoptosis in this paradigm is unknown, but may include an activity-dependent trans-neuronal cascade. The present report examined the effect of adult-onset unilateral naris occlusion, which reduces olfactory bulb afferent excitation of piriform cortex, on apoptosis (terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling [TUNEL]) in the rat anterior piriform cortex. Adult Long-Evans hooded rats received unilateral naris occlusion or a control manipulation and were sacrificed after 1, 5, 7, 10 or 20 days later. For comparison, a second group of rats received a unilateral bulbectomy and were sacrificed 24 h later. Counts of TUNEL-stained cell profiles were performed for layers I/II and layer III of the anterior piriform cortex ipsilateral and contralateral to the manipulation. The results confirmed that unilateral bulbectomy produced a dramatic increase in TUNEL labeling in layers I/II of the ipsilateral piriform cortex 24 h after bulbectomy. Unilateral naris closure also produced enhanced TUNEL labeling, although the magnitude of the effect was less than that produced by bulbectomy, and enhanced TUNEL labeling was apparent both ipsilateral and contralateral to the sealed naris compared to controls. Deprivation-induced TUNEL labeling was detectable by 24 h post-closure, peaked at 5 days and was no different from controls by 20 days post-closure. Neither bulbectomy nor naris closure affected TUNEL labeling in layer III. Together, these results suggest that there is a population of superficial cells in piriform cortex whose survival is tightly regulated by sensory input.
Neonatal olfactory sensory deprivation decreases BDNF in the olfactory bulb of the rat
2001, Developmental Brain Research
We hypothesized that brain-derived neurotrophic factor (BDNF) may be down-regulated in the olfactory bulb ipsilateral to experimental naris occlusion. Unilateral naris occlusion was performed on rats at postnatal day three (P3). On P10, P30, and P60 olfactory bulbs were weighed and assayed for tyrosine hydroxylase (TH), BDNF, and TrkB by Western blotting to determine the response of BDNF and its cognate receptor, TrkB, both during the acute phase of sensory loss (P10) and longer term. TH levels, which are highly dependent on intact input from the olfactory epithelium, were assayed as a means of determining the success of occlusion in each animal. At P10, BDNF protein expression was variable but most often increased ipsilateral to deprivation. In contrast, by P30 and P60 TH levels were found to be significantly decreased in the ipsilateral bulbs as were the levels of BDNF. TrkB protein levels changed little relative to the control side. Immunohistochemical localization of BDNF within the control-side olfactory bulb revealed small cells located mainly in the mitral cell layer and internal plexiform layer. Very few of the BDNF immunoreactive cells were visible in the bulb ipsilateral to the occlusion by P30. Given the roles of BDNF in survival of cells and plasticity during development, the decrease in BDNF expression subsequent to olfactory sensory deprivation may contribute to cellular and synaptic deficits observed by others following olfactory sensory deprivation.
Microglial activation in the developing rat olfactory bulb
2000, Neuroscience
The development of the olfactory bulb, the primary central relay of the olfactory system, is characterized by a striking susceptibility to alterations in the amount of afferent input. For example, blocking airflow through one half of the nasal cavity during early life results in a number of dramatic changes in the bulb, including increased cell death. Previous studies reveal high levels of microglia in the olfactory bulb. Microglia function as phagocytes, aid in synaptogenesis, and produce important trophic and cytotoxic factors. In response to a number of tissue perturbations, microglia undergo an activation process that includes, among other changes, the up-regulation of complement receptor 3. Interestingly, a previous study reported that naris closure had no effect on microglia in the bulb; however, the research did not distinguish the functional activation state of microglia. We further examined the role of microglia in the normally developing and olfactory-deprived rat bulb using immunohistochemical detection of complement receptor 3 as a measure of microglial activation. Expression of the receptor in the bulb is relatively high during postnatal development, in particular when compared to levels in cortical regions caudal to the olfactory bulb. In addition, naris closure performed on the day after birth (but not after the first postnatal month) increases levels of the receptor in an age and laminar-dependent fashion.
The presence of an inducible pool of activated microglia in the olfactory bulb may be important for normal development and contribute to the plethora of changes seen after early olfactory deprivation.
Sensory deafferentation and olfactory bulb morphology in the zebrafish and related species
2000, Brain Research
Citation Excerpt :
This finding has been well established in mammalian species. For example, 30 days of restricted sensory input in 60-day-old rats yields only minor effects in bulb size [45], and in adult mice only a 17% decrease in size [46]. These changes are roughly equivalent to the percent reduction in laminar volumes seen in adult zebrafish and rasbora.
The zebrafish, Danio rerio, has become an important model species for examining olfactory system structure and function, yet little is known about developmental changes in olfactory bulb morphology from embryo to adult. The present study examined both normal growth and the effects of deafferentation on the bulb from hatching to adulthood. In young animals, the bulb is small relative to body size and has a higher percentage of its volume occupied by incoming olfactory nerve fibers. Young animals are also more affected by sensory deafferentation. Olfactory rosette removal resulted in more than 50% reductions in laminar volumes, indicating that sensory input is important during periods of rapid development. In addition, three closely related species were examined to compare how differing bulb morphology might influence the effects of bulb manipulation. The cherry barb, Barbus (=Puntius) titteya, and giant danio, Danio aequipinnatus, have larger bulbs and laminar volumes relative to body size than the zebrafish or scissortail rasbora, Rasbora trilineata. Both are also more affected by deafferentation, with at least a 35% reduction in laminar sizes in many of the bulb layers. The studies are discussed in terms of the importance of the olfactory system to each species and are also compared to the effects of sensory manipulations in other animals.

View all citing articles on Scopus

View full text

Article preview

Brain Research Bulletin

Abstract

References (22)

A versatile and inexpensive planimeter system

J Neurosci Methods

Olfactory bulb maturation in Acomys cahirinus: Is neural growth similar in precocial and altricial murids?

Dev Brain Res

Olfactory granule cell development in normal and hyperthyroid rats

Dev Brain Res

Effects of olfactory deprivation on postnatal growth of the rat olfactory bulb utilizing a new method for production of neonatal unilateral anosmia

Brain Res

A quantitative study of the effects of early unilateral olfactory deprivation on the number and distribution of mitral and tufted cells and the glomeruli in the rat olfactory bulb

Brain Res

Sensory deprivation affects the developing olfactory system of mice

Soc Neurosci Abstr

Sensory deprivation affects mitral cell synapses but not size or number

Soc Neurosci Abstr

Effects of sensory deprivation on the development and maintenance of the olfactory system in mice

Soc Neurosci Abstr

The role of experience in the development of behavior and the nervous system

Continuous nerve cell renewal in the olfactory system

Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia

J Comp Neurol

Cited by (48)

Odorant modulation of neuronal activity and local field potential in sensory-deprived olfactory bulb

Afferent regulation of neuron number in the cochlear nucleus: Cellular and molecular analyses of a critical period

Trans-neuronal regulation of cortical apoptosis in the adult rat olfactory system

Neonatal olfactory sensory deprivation decreases BDNF in the olfactory bulb of the rat

Microglial activation in the developing rat olfactory bulb

Sensory deafferentation and olfactory bulb morphology in the zebrafish and related species