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. Author manuscript; available in PMC: 2023 Sep 1.
Published in final edited form as: Am J Primatol. 2022 Aug 8;84(9):e23427. doi: 10.1002/ajp.23427

Potential trade-off between olfactory and visual discrimination learning in common marmosets (Callithrix jacchus): implications for the assessment of age-related cognitive decline

Elena M Golub 1, Bryce Conner 2, Mélise Edwards 3, Lacey Gilllis 2, Agnès Lacreuse 2,3
PMCID: PMC9444974  NIHMSID: NIHMS1826680  PMID: 35942572

Abstract

Olfactory dysfunction has been identified as an early biomarker for dementia risk but has rarely been assessed in nonhuman primate models of human aging. To better characterize common marmosets as such models, we assessed olfactory discrimination performance in a sample of ten animals (5 females), aged 2.5 to 8.9 years old. The monkeys were proficient in the discrimination and reversal of visual stimuli but naïve to odor stimuli. For olfactory discrimination, the monkeys performed a series of six discriminations of increasing difficulty between two odor stimuli. We found no evidence for an age-related decline as both young and older individuals were able to perform the discriminations in roughly the same number of trials. In addition, the older monkeys had faster responding than the younger animals. However, we noted that when adjusted for age, the speed of acquisition of the first discrimination in the olfactory modality was inversely correlated to the speed of acquisition of their first discrimination of two visual stimuli months earlier. These results suggest that marmosets may compensate for sensory deficits in one modality with higher sensory performance in another. These data have broad implications for the assessment of age-related cognitive decline and the categorization of animals as impaired or non-impaired.

Keywords: marmoset, olfactory, aging, cognition

INTRODUCTION

Over the past two decades, research on olfactory dysfunction in aging and neurodegenerative diseases has grown tremendously. Olfactory dysfunction increases with age (Brai, Hummel, & Alberi, 2020) and is estimated to be present in 14–22% of people over 60 (Boesveldt, Yee, McClintock, & Lundstrom, 2017) and 62–80% of people over 80 years old (Marin et al., 2018). Specifically, the ability of humans to detect, differentiate and identify odors declines with advancing age (Kondo, Kikuta, Ueha, Suzukawa, & Yamasoba, 2020). In addition, the loss of smell is prevalent in many neurodegenerative diseases (Attems, Walker, & Jellinger, 2015; Marin et al., 2018), affecting 96% of patients with Parkinson’s disease (PD) and 90% of patients with Alzheimer’s disease (AD). Olfactory dysfunction precedes the occurrence of symptoms in both AD and PD, highlighting the importance of assessing olfactory function for early diagnosis of these diseases. Additionally, in older adults followed longitudinally (75 years old at study onset), olfactory impairment was identified as the most robust predictor of change in cognitive functioning (MacDonald, Keller, Brewster, & Dixon, 2018).

The molecular, anatomical and cellular pathways supporting incoming olfactory information in humans are well understood (Barresi et al., 2012). The olfactory epithelium, inside the nasal cavity, is comprised of olfactory sensory neurons which express a single type of odorant receptor. All olfactory sensory neurons project to the olfactory bulb, with olfactory sensory neurons expressing odorant receptors converging into structures called glomeruli. Thus they form an odorant receptor map at the surface of the olfactory bulb. The information from this glomerular map is transmitted to the olfactory cortex through projections to multiple areas, including the amygdala, entorhinal cortex and piriform cortex. A number of anatomical changes have been reported in the aging human olfactory system, including age-related decreases in the olfactory bulb volume, the glomerular layer thickness, the number of glomeruli and the concentration of mitral cells (Kondo et al., 2020). In AD, areas that are important to olfactory information processing (i.e., the entorhinal cortex, anterior olfactory nucleus and olfactory bulbs) are among the first to be affected by neurofibrillary tangles (Kondo et al., 2020). As disease progresses, tangles develop in a stereotypical pattern from the entorhinal cortex, perirhinal cortex, hippocampus, and amygdala, before reaching the cortex (Kondo et al., 2020). In PD, the exact mechanisms for olfactory dysfunction are unclear but may involve different neurotransmitter systems (Prediger, Schamne, Sampaio, Moreira, & Rial, 2019).

Diminished olfactory ability with age has been reported in a number of mammals. It is common in dogs over 14 years (Hirai et al., 1996), and has been associated with decreased olfactory receptor neurons and cilia as well as cerebral amyloidosis in the olfactory bulb in older subjects. Data from mice and rats are more variable, suggesting that rodents may be more resistant to age-related changes in the olfactory system. For example, several studies have reported intact olfactory discrimination abilities in aged rats (Barense, Fox, & Baxter, 2002; Kraemer & Apfelbach, 2004; Schoenbaum, Nugent, Saddoris, & Gallagher, 2002). The deficits described in other studies (LaSarge et al., 2007; Prediger, Batista, & Takahashi, 2005; Roman, Alescio-Lautier, & Soumireu-Mourat, 1996) may be due to the type of discrimination involved. Indeed, Yoder et al. (2017) reported that older Fischer F344 rats performed as well as young rats in odor detection thresholds and the ability to discriminate between distinct odors, but had more pronounced deficits when the discrimination involved perceptually similar stimuli, implicating perirhinal cortical dysfunction. In contrast to healthy aging, transgenic mouse models of AD and neurotoxin models of PD are characterized by marked olfactory dysfunction (Prediger et al., 2019).

Given the importance of olfactory dysfunction as a potential early biomarker for later neurodegeneration in older people, as well as potential species differences in the susceptibility to age-related changes in the olfactory system, the phenotypic characterization of nonhuman primate models of human aging ought to include olfactory function. However, very few studies have included such assessments. In one study in the gray mouse lemur, Aujard and Nemoz-Bertholet (2004) assessed testosterone responses to urinary cues in adult (2.3 ±0.3 years old) and aged (6.9 ±0.6 years old) male gray mouse lemurs exposed to urinary odors from pro-estrous females. Following odor exposure, plasma testosterone levels rose in the younger males, but not the aged males. While this finding could be attributed to a decline in testosterone production/sexual arousal, rather than a decline in olfactory function, the authors also gave a discrimination test between water and an odor repellent of varying concentrations. They found that younger subjects avoided the odor repellent at a lower threshold than older individuals, providing support for an age-related olfactory decline. In contrast, Joly, Deputte, and Verdier (2006) found no differences between young (3–4 years old) and old (6–14 years old) gray mouse lemurs in the detection, transfer and reversal learning task of odor stimuli. Unfortunately, the assessment of age-related olfactory impairments in other nonhuman primate species is lacking.

The common marmoset (Callithrix jacchus) has gained interest as a model for human aging (Ross, 2019), due in part to its short lifespan of 10–12 years, which allows for longitudinal investigations (Rothwell et al., 2021). Additional characteristics, such as small size (300–500 g) and ease of breeding make them highly suitable as laboratory animals. In addition, marmosets have a brain architecture typical of primates, with an expanded temporal lobe, highly developed prefrontal cortex and hierarchically structured sensory domains (Fukushima et. al, 2019), which supports a rich social repertoire and cognitive behavior (Samandra, Haque, Rosa and Mansouri, 2022). The marmoset recapitulates several of the neural (Freire-Cobo et al., 2021; Leuner, Kozorovitskiy, Gross, & Gould, 2007), cognitive (Rothwell, Workman, Wang, & Lacreuse, 2022; Sadoun, Rosito, Fonta, & Girard, 2018) and biological (Ross, 2019) changes observed in aging humans. Marmosets are considered old by the age of 8, when such changes become apparent (Abbott, Barnett, Colman, Yamamoto, & Schultz-Darken, 2003).

Minimal anatomical and functional differences between human and marmoset olfaction provide strong support for use of marmosets in olfactory research. Like humans, marmoset olfaction begins in the olfactory epithelium of the main olfactory system and extends to the olfactory bulb. However, marmosets also possess an accessory olfactory system in which pheromonal molecules are received by the vomeronasal organ and transmitted to the accessory olfactory bulb (Moriya-Ito, Tanaka, Umitsu, Ichikawa & Tokuno, 2015). Although the vomeronasal organ is non-functional in humans, the presence of an accessory olfactory system is not directly associated with substantial functional differences in olfaction (Smith & Bhatnagar, 2019). Marmosets have highly developed olfactory systems which are used in a range of behaviors, such as reproduction, avoidance, social interaction and communication, foraging and food selection (Kemp & Kaplan, 2012; Laska, 2015). Marmosets can be trained to detect and respond to diluted odors and discriminate between food and predator-based odors (Kemp & Kaplan, 2012), or reproductive vs. non-reproductive odors. Male marmosets can distinguish between odors from peri-ovulatory vs. non-ovulatory females (Ferris et al., 2004) and peri-ovulatory vs. luteal phase females (Kucklich, Weiss, Birkemeyer, Einspanier, & Widdig, 2019). Olfactory discrimination deficits can be induced experimentally by the toxin MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) in marmoset models of PD (Phillips et al., 2017). Altogether, these data suggest that marmosets are excellent candidates to study age-related changes in olfaction.

The goal of this study was to examine olfactory performance in young and old marmosets, using an olfactory discrimination task of increasing complexity. Secondly, we examined the performance of the animals relative to their prior performance in a visual discrimination task.

METHODS

Subjects

Ten marmosets (5 males, 5 females) participated in this study (Table 1), including 7 older monkeys (mean = 8.07 years old, SD = 0.55, range = 7.48–8.92) and 3 young monkeys (mean = 2.92, SD = .51, range = 2.50–3.50). All subjects were accustomed to performing cognitive tasks on a touchscreen or a manual apparatus (Rothwell et al., 2022). The animals were housed in opposite sex pairs in large vertical cages measuring either (72 × 47 × 29 cm) or (68 × 38 × 30 cm) that contained perches, platforms, a nest box and hammocks. Animals were maintained under a 12 h:12 h dark/light cycle. The ambient temperature was set at approximately 27°C with humidity at around 50% daily. Marmosets were fed Mazuri Callitrichid High Fiber Diet 5M16 (Purina Mills, St Louis, MO) in addition to a variety of fresh fruits, nuts, seeds and mealworms. Fruit and nuts were provided twice daily (8–9 AM and 1–3 PM) and water was available ad libitum. The monkeys were provided with daily enrichment, including foraging tubes and a variety of toys. Animals were cared for in accordance with the guidelines of the US National Research Council’s Guide for the Care and Use of Laboratory Animals, and the US Public Health Service’s Policy on Humane Care and Use of Laboratory Animals (2011), 8th edition. The studies were approved by the University of Massachusetts Institutional Animal Care and Use Committee. All authors adhere to the American Society of Primatologists Principles for the Ethical Treatment of Non-Human Primates.

Table 1.

Marmosets’ characteristics and Trials to Criterion (TTC) for the Visual and Olfactory initial discriminations.

Subject Sex Age at Visual Testing onset (years) TTC Visual Age at Odor Testing Onset (years) TTC Odor
1 F 1.82 195.00 2.50 328.00
2 M 2.24 364.00 2.76 58.00
3 M 1.82 137.00 3.50 444.00
4 F 6.96 141.00 7.48 281.00
5 F 7.00 265.00 7.55 576.00
6 M 7.36 55.00 7.88 445.00
7 F 7.34 464.00 * 7.95 346.00
8 M 7.47 207.00 8.05 730.00
9 F 8.17 751.00 8.73 88.00
10 M 8.39 194.00 8.92 848.00
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*

performed on WGTA

Olfactory task

Apparatus Design

The olfactory task was initiated between September 2019 and November 2019 for all but one monkey who started the experiment later (November 2020). The custom-made testing apparatus consisted of a transparent Plexiglas panel (31 × 24.5 cm) with 2 bottom openings (4 × 5 cm) and a flat sliding board (22 × 15 × 1.5 cm). For testing, the apparatus was affixed to the front of a regular marmoset transport box (34.1 × 20.65 × 30.8 cm; Figure 1). The sliding board contained 2 wells (7.5 cm apart) for presentation of scent containers (1.7 × 4.5 cm). Before presentation of the stimuli a scented cotton pad was placed inside each container, outside the view of the monkeys. The container tops were perforated to allow for the marmosets to smell the stimuli without tampering with the containers. For stimuli presentation, the experimenter placed each container in a well and slid the board through the openings, toward the monkey’s side (Figure 2). The monkeys were tested in their housing room among other monkeys. The olfactory discrimination task consisted of an habituation period, followed by 6 successive discrimination phases of increasing difficulty.

Figure 1.

Figure 1.

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The olfactory discrimination apparatus affixed to a transport box

Figure 2.

Figure 2.

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A marmoset performing the olfactory discrimination task (left) and the visual discrimination task (right). Bottom: pair of stimuli used for the visual discrimination

Habituation

Prior to testing, the marmosets were habituated to the stimuli through instrumental conditioning. While in the home cage, they were first rewarded for overtly sniffing a maple scented container presented to them by an experimenter. Once the animals were consistently sniffing the container (i.e., 10/10 trials), training with the odor apparatus started. Monkeys were placed in a transport box fitted with the apparatus. A single scent container containing maple scent extract was presented either in the left or right position of the testing board and marmosets were required to overtly sniff the scent container to be rewarded with a mini dried marshmallow. Next, they had to sniff and push the container toward the experimenter to retrieve a marshmallow underneath. In order to prevent subjects from pushing the scent containers before sniffing, experimenters held the scent containers in place until sniffing occurred.

Testing

Once the monkeys learned “the sniff and push” behaviors, they were tested in six experimental phases with two containers presented side by side. The scents used for discrimination were maple and lemon scent extracts of different concentrations. The rewarded stimulus (i.e., maple scent) was randomly placed to the left or right position of the board, according to a specific test sheet which randomized the location of each container. The 6 phases included: maple vs. no scent; 3 drops maple versus 3 drops lemon, 1 drop of both scents, 1:25 dilution of both scents, 1:50 dilution of both scents and a 1:100 dilution of both scents. Monkeys were given 20 trials per testing session until they reached 18/20 trials, or a 90% learning criterion. For each trial, they were given a maximum of 60s to respond, after which the trial was recorded as an omission and the next trial was delivered. If the monkey pushed the correct stimulus, they were rewarded with a mini dried marshmallow underneath. If they selected the incorrect stimulus, they were not rewarded and the next trial was administered. The response times, corresponding to the time elapsed between stimuli presentation and a push on either stimulus, were recorded with a stop watch for each trial. Once 90% of trials were correctly selected, the monkey was tested in the following experimental phase. If the monkey was unable to reach criterion within 1000 trials for a specific phase, they were removed from subsequent testing.

Visual task

As part as a longitudinal study on aging, the monkeys had performed a series of yearly visual discrimination and reversal tasks on touchscreen (Monkey CANTAB Intellistation with Liquid Reward, Model 80951A) or a manual version before participation in the odor task (Rothwell et al., 2022). For the purpose of the current study, performance on the first visual discrimination (before any reversal) that monkeys performed closest to the olfactory task was considered. For all monkeys but one, the olfactory task was performed within 8 months (range 5–8) of the Visual task. For one monkey, the time interval between the two tasks was 20 months. For visual testing, monkeys voluntarily entered a transport box (34.1 × 20.65 × 30.8 cm) attached to the front of their homecage to access the CANTAB apparatus (see LaClair et al., 2019 for details). They were presented with two stimuli (Figure 2) that appeared in any position on the touch screen. Upon touching the correct stimulus, a positive tone was played and a liquid reward (banana milkshake) was delivered. Touching an incorrect stimulus triggered a negative tone and no reward delivery. The inter-trial interval was 3 seconds. Animals were tested 5 days a week and were given 40 trials a day to learn the stimulus/reward contingencies until a 90% correct criterion. The number of trials needed to reach a 90% correct learning criterion was the main dependent variable. One monkey was tested on a manual version of this test, in which similar physical stimuli were presented in a Wisconsin General Testing Apparatus (WGTA). Visual discrimination performance does not differ the two platforms, although response times are typically longer in the WGTA (Rothwell et al., 2022).

ANALYSIS

Several dependent variables were used to describe performance on the olfactory discrimination task: the number of trials to reach criterion (TTC), the number of errors to reach criterion (Errors) and the response times (RT). One older monkey who performed the visual task on WGTA was excluded from analyses involving RT, as responses on WGTA were significantly slower than those on touchscreen, due to task requirements. Prior to analysis, the raw data were log transformed to reduce skewness and meet the assumptions of normality. Age entered as a categorical variable in the models due to its bimodal distribution between young and old subjects. Each outcome (TTC, Errors and RT) was analyzed using linear mixed models, with Age category (young, old) and Phase (1–6) as factors, and subject ID as a random effect. The association between TTC olfactory and TTC visual was examined with a partial correlation controlling for age at the time of olfactory testing.

RESULTS

Olfactory discrimination task

To facilitate interpretation, all figures represent the raw data. Figure 3 depicts the mean TTC as a function of Phase and Age category for the olfactory task. All monkeys were able to acquire the scent vs. non-scent discrimination, with two of the 3 young monkeys and 5 of the 7 older monkeys successfully completing the 5 subsequent discriminations. The linear mixed model for TTC revealed no effect of Age (F(1, 16.28) = 0.10, p = 0.75), Phase (F(5, 34.47) = 1.46, p = 0.23), or their interaction (F(5, 34.47) = 0.75, p = 0.59). Similarly, the number of errors did not significantly differ as a function of Age (F(1, 15.79) = 0.06, p = 0.80), Phase (F(5, 35) = 2.21, p = 0.07), or their interaction (F(5, 35) = 1.06, p = 0.40). However, a main effect of Age was found for RT (F(1, 11.16) = 5.33, p = 0.04), while the effects of Phase (F(5, 31.73) = 0.34, p = 0.88) and Phase x Age (F(5, 31.73) = 2.13, p = 0.09) were not significant. This indicated that, independent of Phase, the older monkeys [M = 9.30, 95% C.I. (7.92, 10.91)] responded faster than the young monkeys [M = 12.81; 95 % C.I. (9.87, 16.61; Figure 4]. Additionally, slower RT was significantly associated with higher TTC (r (6) = - 0.55, p = 0.03), but not the number of errors (r (6) = - 0.52, p = 0.18), when controlling for age. This finding indicated that responses slowed down as a function of the number of trials needed to reach the criterion, suggesting that RT was associated with some aspects of task difficulty.

Figure 3.

Figure 3.

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Trials to criterion (A) and Errors to criterion (B) as a function of phase and age category.

Figure 4.

Figure 4.

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Response times as a function of phase in old and young marmosets.

Comparison with a prior visual discrimination task

All monkeys performed a series of yearly discriminations and reversals of visual stimuli as part as a longitudinal study on aging (Rothwell et al., 2022). We analyzed performance on the first visual discrimination that monkeys performed closest to the olfactory discrimination task. For all but one monkey, the two tasks were performed on the same year, within 6 to 8 months of each other. One young monkey with the same amount of visual testing was added to the olfactory task later, with 20 months separating the two tasks (see Table 1). We noticed that monkeys who had been particularly slow in acquiring this initial visual discrimination, were fast in acquiring the olfactory discrimination and vice versa. To investigate this relationship further, we performed a partial correlation between TTC olfactory and TTC visual, controlling for chronological age at the time of olfactory discrimination. We found that TTC olfactory was inversely correlated with TTC visual (r (7) = - 0.69, p = 0.041), when controlling for age; Figure 5). This indicated that the monkeys who acquired the visual discrimination quickly, tended to perform poorly on the olfactory discrimination and vice versa. In addition, within the older monkeys, the magnitude of the TTC score difference (absolute values) between the visual and olfactory task increased significantly with age (r(7) = 0.83, p = 0.019) indicating that the older the monkeys were, the larger the performance difference between the two modalities.

Figure 5.

Figure 5.

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Scatterplot of the relationship between Trials to criterion (TTC) olfactory and TTC Visual.

DISCUSSION

We examined olfactory discrimination abilities in old and young marmosets using two odor stimuli which were increasingly diluted and therefore progressively more difficult to discriminate. Our sample was small, but we found no evidence for age differences in olfactory discrimination capabilities, as monkeys from both groups were able to perform the 6 discriminations in roughly the same number of trials and errors. Unexpectedly, the RT were overall faster in older monkeys than younger ones. This finding is counter-intuitive in light of the well-documented age-related slowing of motor function (Zhang et al., 2000) and speed of processing (Salthouse, 1996) observed in humans and other primates. Importantly, faster RT was associated with faster acquisition of the task (as measured by TTC) when controlling for age, suggesting that RT captured some aspects of task difficulty and/or motivation.

Importantly, an inverse relationship was found between the speed of acquisition of discrimination learning in the olfactory vs. visual modality, so that, controlling for age, monkeys who quickly acquired the olfactory discrimination were slow in acquiring the visual discrimination, and vice versa. In addition, the magnitude of the difference in TTC between the two modalities increased with age in older animals. These results suggest that marmosets may somewhat compensate for sensory deficits in one modality with higher sensory performance in another. These data have broad implications for the assessment of age-related cognitive decline and the categorization of animals as impaired or non-impaired.

The importance of assessing sensory function in age-related cognitive decline cannot be overstated (Whitson et al., 2018). Changes in sensory processing are a hallmark of normal aging and sensory impairments are risk factors for age-related cognitive decline and dementia (Baltes & Lindenberger, 1997; Lindenberger & Baltes, 1994; Murphy, 2019; Roberts & Allen, 2016), with evidence for hearing loss (Lin et al., 2011), visual impairment (Lin et al., 2004) and olfactory deficit (Murphy, 2019; Wilson et al., 2009) associations. Sensory impairments have most often been studied in isolation, but several factors highlight the importance of considering multiple sensory assessments for cognitive and neurodegenerative diseases. First, impairment in one sensory domain does not necessarily imply impairment in another sense. For example, Cavazzana et al. (2018) tested sensory threshold across the 5 senses in older people and found that only auditory function exhibited a significant age-related decline. Second, the relationship between sensory impairment and cognitive impairment may not be unique to one sensory system. In Fischer et al. (2016)’s longitudinal study, hearing, visual, and olfactory deficits, independent of one another, had significant effects on 10-year risk of cognitive impairment. Third, studies in animal models of cognitive aging, and particularly nonhuman primate studies, have largely neglected to assess sensory function along with cognitive assessments. Yet, visual acuity (Fernandes, Bradley, Tigges, Tigges, & Herndon, 2003), auditory processing (Gray & Barnes, 2019; Sun et al., 2021) and olfactory function (Aujard & Némoz-Bertholet, 2004) all decline with age in nonhuman primates. Assessing sensory function in concert with cognitive function in the same animals is crucial for a better understanding of individual differences in aging. For example, Gray and Barnes (2019) showed that older rhesus monkeys with better auditory processing performance had overall higher cognitive function.

Finally, the broader implications of our findings in marmosets, is that individuals performing poorly in one modality (i.e., visual), may not be considered impaired if performance in another modality (i.e, olfactory) is taken into account, perhaps in part due to compensatory mechanisms. Compensatory mechanisms have been well documented in people with congenital sensory deficits. For example, blind individuals have been found to have superior abilities in intact modalities, including tactile, auditory and olfactory (Chinnery & Thompson, 2015; Cuevas, Plaza, Rombaux, De Volder, & Renier, 2009; Hoover, Harris, & Steeves, 2012; Levänen & Hamdorf, 2001), and visual areas of the brain are recruited during the spatial processing of auditory stimuli in blind individuals (Hoover et al., 2012). Similarly, there is evidence that deaf individuals perform better than hearing people in specific visual tasks (Bavelier, Dye, & Hauser, 2006). Recent studies also show sensory compensation to be present in those with anosmia. For example, individuals with acquired or congenital anosmia show enhanced performance in an audio-visual simultaneity judgement task when compared to controls and enhanced activation of a multisensory ROI in the superior temporal sulcus (Peter et al., 2021; Peter, Porada, Regenbogen, Olsson, & Lundstrom, 2019).

To our knowledge, however, the idea of sensory compensation in normal aging has received very little attention. One study tested this idea by comparing visual acuity and cognition in older adults with and without hearing loss (Wettstein, Wahl, & Heyl, 2018). The results showed that visual acuity predicted cognitive functioning only in people with hearing loss, suggesting that visual acuity compensated for the hearing impairment in order to maintain cognitive ability in this older population.

Our findings suggest that some level of compensation may occur in older marmosets, as the difference in learning scores between the visual and olfactory modality increased linearly with age. However, marmosets rely heavily on olfactory function for a wide range of behaviors spanning reproduction, communication and foraging (Kemp & Kaplan, 2012; Laska, 2015) and the results cannot disentangle the role of motivation or attention from those of associative learning ability in mediating these effects. In addition, it is unclear how these findings in marmosets may generalize to other primate species with less developed olfactory function.

Finally, our interpretation is mitigated by several limitations, including a small sample size, with unbalanced age and sex groups. Perhaps more importantly, our observations were post-hoc and the order of tasks not controlled for. Finally, the different testing set-ups (touchscreen for visual vs. manual apparatus for olfactory) may have played a role. Therefore, additional empirical support is needed to more convincingly demonstrate compensation between the olfactory and visual modalities in old age. Nevertheless, we suggest that characterizing subjects as impaired or non-impaired on the basis of learning in a single sensory modality may not capture the full spectrum of the aging phenotype. Future studies will need to incorporate comprehensive assessments of sensory changes, along with assessments of cognitive, motor, behavioral and neural changes, for understanding how the brain may compensate for the functional decline that accompany the aging process.

Research Highlights.

  • Young and older marmosets performed similarly in an olfactory discrimination task, but older monkeys had faster responding

  • Marmosets who quickly acquired the initial olfactory discrimination were slow to acquire an initial visual discrimination and vice versa.

  • In older monkeys, the difference in learning scores between the visual and olfactory discrimination increased with age

  • Marmosets may compensate for sensory deficits in one modality with higher sensory performance in another.

ACKNOWLEDGMENTS

This study was supported by NIH R01 AG046266. We are grateful to all the laboratory members who participated in animal training and testing. We thank the UMass Psychology shop for building the olfactory apparatus and the veterinary and animal care staff for their excellent care of the marmosets. The authors have no conflict of interest to declare. The data are available upon request.

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