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Sensory Cueing of Autobiographical Memories in Normal Aging and Alzheimer’s Disease: A Comparison Between Visual, Auditory, and Olfactory Information

Background: Alzheimer’s disease (AD) is a chronic, neurodegenerative disease resulting in a progressive decline of autobiographical memories (AMs) which favors the development of psycho-behavioral disorders. One of the most popular psychosocial interventions in dementia care, Reminiscence Therapy, commonly uses sensory cueing to stimulate AMs retrieval. However, few empirical studies have investigated the impact of sensory stimulation on AMs retrieval in AD. Objective: Our goal was to determine the most relevant cue for AMs retrieval in patients with early to mild AD when comparing odors, sounds and pictures. Methods: Sixty AD patients, 60 healthy older adults (OA), and 60 healthy young adults (YA) participated in our study. Participants were presented with either 4 odors, 4 sounds, or 4 pictures. For each stimulus, they were asked to retrieve a personal memory, to rate it across 3 dimensions (emotionality, vividness, rarity) and then to date it. Results: Overall, results showed no clear dominance of one sensory modality over the others in evoking higher-quality AMs. However, they show that using pictures is the better way to stimulate AD patients’ AM, as it helps to retrieve a higher number of memories that are also less frequently retrieved, followed by odors. By contrast, auditory cueing with environmental sounds presented no true advantage. Conclusion: Our data should help dementia care professionals to increase the efficiency of Reminiscence Therapy using sensory elicitors. Other clinical implications and future directions are also discussed.

visual dominance. For this reason, we choose to prioritize the selection of the best representative sounds and/or odorants.
We were provided with 8 odorants, evoking 8 different items: fresh laundry, apple, fresh-cut grass, coffee, wood fire, toasted bread, wine, and piggery. Following Herz procedure [1], we originally aimed to select an auditory and a visual version for each of these items, so that each item was eventually available in 3 different sensory forms (e.g., a picture of the sea, the sound of the waves, and the smell of the sea).

Pilot 1: Assessment of Items' Sensory Properties
Participants Twenty-four young adults (18 females, Mage 23.9 years, SD 3.4) and 25 older adults (19 females, Mage 75.1 years, SD 6.7) took part in the experiment. All reported normal vision and had no neurological or psychiatric history. Participants gave their written informed consent.

Materials and procedure
We asked participants to rate the 8 items presented in 3 different sensory forms (olfactory, auditory, and visual) so that a total of 24 different sensory stimuli were tested. The stimuli were delivered on a computer using E-Prime ® 2.0 software. The stimuli were presented in three different blocks (odor block, sound block, and picture block). Order of presentation of both blocks and stimuli were counterbalanced across subjects. Visual stimuli consisted of 8 digital pictures (640x480 pixels) of the items shown on a black background. Auditory stimuli were 8 recording samples of ecological noises. Each audio file lasted approximatively 10 s and was played through speakers at either side of the computer screen. Olfactory stimuli were 8 fragrances provided by International Flavors & Fragrances Inc. They were presented by using sniffing sticks (provided by Burghart Messtechnik, Germany) that were handed to the participants by the experimenter following the E-Prime instructions.
For each stimulus, participants were first asked to identify the item by naming it (e.g., [the smell of/the sound of/the picture of] the sea). Immediately after the response, the real identity of the item was revealed and participants were then asked to rate the stimulus on 3 scales: representativeness (how accurately the stimulus represented the real item) on a 9-points Likert scale (1 = not at all, 9 = extremely); pleasantness, on an 11-points Likert scale (-5 = extremely unpleasant, 5 = extremely pleasant); intensity (for olfactory and auditory stimuli only), on a 6points Likert scale (0 = not at all intense, 5 = very intense).

Descriptive statistics and results
For each stimulus, we calculated (i) the percentage of correct responses, (ii) the mean representativeness score, (iii) the mean pleasantness attributed by the participants, and (iv) the mean intensity (exclusively for olfactory and auditory stimuli). Results are reported graphically in Supplementary Figures 1a and 1b.

Pilot 2: Assessment of Items' Conceptual Properties
In Pilot 2, the same 8 items were evaluated on a conceptual dimension.

Participants
A total of 24 young adults (18 females, Mage 24.6 years, SD 6.7) and 21 older adults (19 females, Mage 74.4 years, SD 3.6) took part in the experiment. All reported normal vision and had no neurological or psychiatric history. Participants gave their written informed consent.

Materials and procedure
Participants filled out a 5-minute questionnaire developed specially for this study. They were asked to rate the most common descriptors (i.e., words) related to each sensory form in which each item was presented in Pilot 1 on several dimensions. For instance, in Pilot 1, we asked participants to evaluate the item "Coffee" by presenting it in the odor form (i.e., the smell of coffee), in the auditory form (i.e., the noise made by a coffee machine) and in the visual form (i.e., a picture of a cup of coffee). Then, in Pilot 2, we asked our participants to evaluate the following descriptors: "Coffee", "Coffee machine" and "Cup of coffee". However, in some cases, the same descriptor could be easily associated with two or more sensory forms; this was the case for the item "Wood fire" or "Apple". Thus, a total of 17 descriptors was evaluated (see Supplementary Table 1). Participants were asked to rate each descriptor on 4 dimensions: evocativeness (the number of memories each descriptor evokes), on a 4-alternative forced-choice label scale (options: "None", "Just one", "A few" and "A lot"); concreteness, on a 6-points Likert scale (0 = "Not concrete at all", 5 = "Very concrete"); pleasantness, on an 11-points Likert scale (-5 = extremely unpleasant,

Descriptive statistics and results
Participants' responses for the evocativeness assessment were coded using a 4-points scale.
We attributed 0 points to the response "None"; 1 point to "Just one"; 2 points to "A few"; 3 points to "A lot". For each stimulus, we computed mean scores for evocativeness, concreteness and pleasantness. Results are reported graphically in Supplementary Figure 2a and 2b.

Phase 2: Stimuli Selection
As expected, regarding items' olfactory forms on a sensory dimension, perfect Representativeness was extremely hard to achieve. Thus, as stated above, we prioritized the selection of the best representative olfactory stimuli. We decided to exclude olfactory stimuli that obtained ≤ 50% correct responses at the identification task and a mean rating score ≤ 5 on the Representativeness scale (Supplementary Figure 1a and 1b).
We also decided to break the link across the items' sensory forms, i.e., we took the liberty to select different items for each modality. We kept the 4 olfactory stimuli with the best Representativeness score. After several trials, we considered the selection presented in Table 3 as the most relevant one. In this final selection, Auditory and Visual stimuli shared the same item selection and stimulus descriptors (i.e., bread, apple, wood fire, and wine). The link across the different sensory forms was preserved only for the item "Apple".

Representativeness
The ANOVA showed a main effect of Group (F(1,141) = 36.3; p < 0.001; η 2 p = 0.20), as YAs rated our stimuli higher than OAs on this variable. We also observed a main effect of Sensory form (F(2,141) = 49.6; p < 0.001; η 2 p = 0.41). Pictures were still judged to best represent real objects, followed by Sounds and Odors. All pairwise comparisons were significant. An interaction between Group and Sensory form was also found (F(2, 141) = 13.7; p < 0.001; η 2 p = 0.16). Again, almost all the pairwise comparisons were significant. However, interestingly, YAs only perceived a difference between Odors and Pictures in their representativeness of the real objects. Lastly, YAs and OAs did not differ in their assessment of Pictures' representativeness.

Pleasantness
The ANOVA showed a main effect of Group (F(1,141) = 8.38 ; p < 0.01 ; η 2 p = 0.05) revealing that OA judged our stimuli as globally more pleasant than YA. We also observed a main effect of Sensory form (F(2,141) = 13.41 ; p < 0.001 ; η 2 p = 0.15). Pictures were still rated as the most pleasant sensory form, followed again by Odors and Sounds 1 . However, this time 1 , post-hoc analysis revealed that Sounds were rated as significantly less pleasant than Pictures only, while no differences were observed when comparing with Odors. The significant interaction between Group and Sensory form (F(2, 141) = 7.13 ; p < 0.01 ; η 2 p = 0.09) and subsequent post-hoc results' analysis showed that: (i) Sounds were now 1 judged as pleasant as Odors, but not Pictures, by OA, while they were still rated as less pleasant than both Odors and Pictures by YA, (ii) Odors were as pleasant as Pictures for YA and (iii) there was still 1 no differences between YA and OA in rating our Odors pleasantness.

Intensity
The ANOVA performed on Odors' and Sounds' intensity showed no main effects nor interaction (all F < 2; all p > 0.1).

Evocativeness
The ANOVA showed a main effect of Group (F(1,88) = 25.7; p < 0.001 ; η 2 p = .22) as OA judged our overall set of stimuli globally more evocative than YA. However, this time 1 we observed no other main effect or interaction (all F < 1; all p > .1), suggesting that the Sensory forms shared an equivalent degree of evocativeness across groups.

Pleasantness
The ANOVA showed a main effect of Group (F(1,88) = 30.6; p < 0.001; η 2 p = 0.25), as OAs judged our stimuli as more pleasant than YAs. No other main effects or interactions (all F < 2; all p > 0.1) were observed, indicating that all Sensory forms were perceived as equally pleasant across groups.

Concreteness
The ANOVA showed no main effects nor interactions (all F < 2; all p > 0.1), suggesting that all stimuli were perceived as equally concrete across groups and Sensory forms.

General Discussion
Our final selection displays two critical strengths: (i) on the Sensory dimension, Sounds were perceived equally pleasant as Odors, (ii) perfect inter-modality matching was obtained in the Conceptual dimension, for each property (Evocativeness, Pleasantness and Concreteness), separately for YAs and OAs.
Setting aside the differences in Representativeness driven by visual dominance, we found noteworthy that our Olfactory and Auditory stimuli were still judged as equally representative of the real items by YAs (i.e., in young, normal cognition). Moreover, importantly, Odors and Sounds showed no significant differences in Intensity in the Sensory dimension, for both groups, nor in Pleasantness, regardless of the dimension.
In sum, after a long phase of pretesting, the final selection was the most satisfactory for our inter-subject design. In the Sensory dimension, overall, our stimuli were considered as mildly to highly representative of the real items, as well as mildly pleasant and intense. Importantly, Odors and Sounds were rated similarly on Pleasantness across our participants but also on Representativeness by YAs. They were also perceived as equally intense by both YAs and OAs.
In the Conceptual dimension, perfect inter-modality matching was obtained for each property (i.e., Evocativeness, Pleasantness and Concreteness), and separately for YAs and OAs. Our stimuli were perceived as mildly concrete, mildly pleasant and evocative across the different sensory forms.
However, crucially, no interaction between Group and Type of sensory stimulation was found (F(4, 170) = 1.45; p = 0.21; η 2 p = 0.03), indicating that, overall, our 3 groups of participants perceived a similar magnitude of association between the different sensory stimuli and the real objects they were meant to represent.

Intensity
The ANOVA performed on Odors and Sounds intensity with Type of sensory stimulation (Olfactory/Auditory) and Group (AD/OA/YA) as between-subjects factors showed no main effects (all ps > 0.1). Our stimuli shared a similar perceived intensity across our groups (mean = 4.02 ± 1.16, 3.79 ± 1.16, and 3.61 ± 1.05 for YA, OA, and AD patients, respectively) and both sensory modalities (mean = 3.75 ± 1.09 and 3.86 ± 1.17 for Odors and Sounds, respectively).