Elsevier

Physiology & Behavior

Volume 81, Issue 4, June 2004, Pages 639-644
Physiology & Behavior

Response to urinary volatiles and chemosensory function decline with age in a prosimian primate

https://doi.org/10.1016/j.physbeh.2004.03.003Get rights and content

Abstract

The age-related decline in olfaction is well documented in humans. However, no data are available to date on changes in olfactory sensitivity with age in nonhuman primates. In the male gray mouse lemur (Microcebus murinus), a prosimian primate, the sense of smell is of high relevance for the modulation of both behavioral and physiological functions. We first assessed the effect of aging on physiological responses to urinary cues by measuring reproductive function in adult and aged males exposed to urine odor of preoestrous females. We then evaluated the effect of aging on chemosensory function using a discrimination test in freely behaving animals. Our results indicate that whereas adult animals show a clear increase in testosterone levels when exposed to female urine odor, this effect is lacking in aged animals. In addition, chemosensory function shows a progressive decline with age. Using both physiological responses to urinary volatiles and spontaneous behavior, this study provides the first data set on the effect of aging on chemosensory responsiveness in a nonhuman primate.

Introduction

Age-related changes have been reported in all sensory systems studied to date. Decrements occur in sensory modalities, such as vision, hearing, taste, olfaction, vestibular function and somatosensation [3], [9], [17]. Although it is often not considered as important as vision or audition in humans, age-related olfactory dysfunction raises increasing interest due to its impact on quality of life and its significant prevalence in some types of pathological aging, such as Alzheimer's disease [12], [13], [16]. Olfactory dysfunctions have been widely reported for elderly humans [22], [26]. Mechanisms accounting for the functional and anatomical deteriorations of the sense of smell with physiological aging are not yet entirely elucidated, because the structure of the olfactory epithelium appears altered with age [21] but its regenerative capacity seems to be relatively well preserved [11]. The declines in sensory function often reflect the combined effect of age-related changes in both the sensory organ and the central nervous system processing of sensory information, leading to a wide range of investigation when looking for underlying mechanisms.

Because of their well-defined and fundamental actions on organism biology and behavior, pheromones serve as powerful tools with which to investigate olfactory function (for review, see Ref. [28]). In this respect, chemical signals mediated through chemosensory pathways appear to be fundamental to many aspects of mammalian reproductive biology. Studies have been mainly performed on rodents, in which the importance of chemosensory cues in mediating reproductive function has been widely investigated (for review, see Ref. [32]). With regard to aging processes, a decrease in the stimulatory effect of male urine has been demonstrated in aged female rats [31]. In contrast to rodents, comparative studies on aged nonhuman primates are unfortunately unavailable to date, especially because of the long life span of most primates and also because of the difficulty to investigate behavioral and physiological patterns associated with olfactory stimulation.

The present study was undertaken in a prosimian primate, the gray mouse lemur (Microcebus murinus, Cheirogaleidae, Primates). This nocturnal and arboreal primate has highly developed sensory modalities to ensure adaptive locomotor and feeding behaviors in dense forest biotope (jumping, climbing and catching of insects) but also social communications between solitary living individuals. In this species, like in many prosimian primates and some simian primates [7], [8], [33], the sense of smell is of high relevance for the modulation of both behavioral and physiological functions. Social communication mainly relies on chemical signals actively dispersed by mouse lemurs through typical marking behaviors, such as urine washing [19], [23]. Chemosensory structures include main olfactory bulbs and a functional vomeronasal organ. These structures are especially developed reaching more than 2.6% of the cerebral mass, compared to an average of only 0.13% in simians [2]. Moreover, this species so far provides the unique example within primates of the presence of true pheromones acting on sexual physiology [25]. Chemical cues from urine affect reproductive function in both sexes and chemocommunication is clearly involved in regulating sociosexual behavior, especially intermale competition for priority access to mating with receptive females [17], [18].

There are some arguments to believe that the chemosensory system is altered with aging in the mouse lemur. First, aged male mouse lemurs show a decrease in the frequency of sniffing and licking of the genitalia of receptive females and also a decrease in the frequency of scent-marking behaviors [1]. Second, aged mouse lemurs exhibit a decrease in the frequency of exploratory behavior in the open-field test [15]. However, an estimation of the age-related decline in chemosensory sensitivity is needed to clarify if the chemosensory system is involved in these processes.

Therefore, this study was performed in two steps. First, because exposure to urinary signals leads to typical physiological and behavioral responses that can be easily monitored in this primate, a noninvasive experimental procedure was used to investigate the effect of aging on the stimulation of reproductive function by urinary volatiles in mouse lemurs. Second, a behavioral study was designed to evaluate the chemosensory preference threshold in freely behaving animals.

Section snippets

Materials and methods

All animals used in this study were born and raised in captivity at the Laboratory of General Ecology (Brunoy, France, license approval N° A91.114.1). As already described [18], conditions of captivity were maintained constant (ambient temperature of 25 °C, hygrometry of 55%). Mouse lemurs are photoperiod-dependent seasonal breeders exhibiting complete gonadal regression and low testosterone levels during exposure to short days (less than 12 h of light per day) and full sexual activity and high

Results

As shown in Fig. 1, during the period of sexual activation, chronic exposure to urine odor from sexually attractive females induced a significant increase in the testosterone levels of adult male mouse lemurs at Week 2 [t(18)=−12.0, P<.05]. Testosterone levels were also significantly elevated at Week 4 [t(18)=−8.0, P<.05]. By contrast, aged male mouse lemurs exposed to the same chemical stimulation did not show any significant increase in testosterone levels compared to control aged males,

Discussion

Our data indicate that the increase in plasma testosterone levels of adult mouse lemurs following exposure to urinary volatiles is lacking in older individuals. In addition, chemosensory function shows a progressive decline with age. Using both physiological responses to urinary volatiles and spontaneous behavior, this study provides the first data set on the effect of aging on smell function in a nonhuman primate.

In mouse lemurs, whereas urine odor stimulation led to a rapid and stable

Acknowledgements

The authors are grateful to A. Schilling for providing the equipment and to M. Perret for helpful comments.

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