The use of an olfactometer for directly presenting odorants opens exciting opportunities for researchers of olfactory memory. The current paper discusses issues related to this methodology as related to a previously published experiment on olfactory context dependent memory.
Information is retrieved more effectively when the retrieval occurs in the same context as that in which the information was first encoded. This is termed context dependent memory (CDM). One category of cues that have been shown to effectively produce CDM effects are odors. However, it is unclear what the boundary conditions of these CDM effects are. In particular, given that olfaction has been called an implicit sense, it is possible that odors are only effective mnemonic cues when they are presented in the background. This assertion seems even more likely given that previous research has shown odors to be poor cues during paired associate memory tests, where odors are in the focus of attention as mnemonic cues for other information. In order to determine whether odors are only effective contextual mnemonic cues when presented outside the central focus of an observer, an olfactory CDM experiment was performed in which odorants were presented directly, rather than ambiently. Direct presentation was accomplished with the aid of an olfactometer. The olfactometer not only allows for direct presentation of odorants, but provides other methodological benefits, including the allowance of trial by trial manipulations of odorant presentations and, relatedly, time-specific releases of odorants. The presence of the same odor during both encoding and retrieval enhanced memory performance, regardless of whether the odor was presented ambiently or directly. This finding can serve as a basis for future olfactory CDM research which can utilize the benefits of direct presentation.
Retrieval is enhanced when it occurs in the same context as encoding1,2; this is termed context dependent memory (CDM). Many stimuli have been shown to be effective contextual cues for enhancing retrieval3. In line with this general research, it has been shown that information that is learned and retrieved in the presence of the same odor is remembered better than information that is retrieved in the presence of a different odor4 or information that is neither learned nor retrieved in the presence of an extra olfactory context5; this has been termed olfactory context dependent memory (OCDM).
The use of odors as contextual mnemonic cues provides researchers with new opportunities to investigate various questions related to both CDM and olfactory processing. Indeed, the relationship between olfaction and memory has been shown to be unique6,7,8. Memories for odors seem to be more resistant to forgetting than memory for other stimuli6 (though this is not always found9). Furthermore, autobiographical memories that are cued by odors are experienced differently than autobiographical memories cued by other stimuli7.
There are other interesting differences between olfaction and the "major" (i.e., visual and auditory) senses. For example, when humans see or hear stimuli, we are frequently able to explicitly identify them and we often consciously adjust our behavior in line with the information they present. However, we are frequently unable to identify odors10. Furthermore, although humans are constantly surrounded by odorous substances, we do not always have the conscious experience of perceiving an odor. Accordingly, it has been proposed that olfaction is an implicit sense, and that odors mostly influence our behavior when we do not consciously perceive them11.
If olfaction truly is an implicit sense, it poses the question as to whether odors must necessarily be outside the focus of awareness for them to act as effective contextual mnemonic cues. Some evidence would suggest this is the case, as odors have been shown to be less effective cues in paired-associates paradigms then other stimuli12,13. To this point all studies that have shown evidence of OCDM have utilized ambient presentation of odorants, whereby the odorants are presented in the background and subjects learn some other target information4,14. Often, the subjects are never explicitly told about the odors.
The focus on ambient odorant presentation up to this point has been logical, as odorants are generally present in the background of an experience, but odors are infrequently at the center of our attentional focus. That being said, ambient odorant presentation necessarily means that researchers relinquish control over some aspects that may be of interest. Chief among these aspects is time. With ambient presentation odorants must be present for a long period of time, with no control over the moment of presentation or odor perception. However, presenting odorants directly, for example with the aid of an olfactometer, allows the researcher to manipulate the time of the odorant presentation in relation to the onset time of other stimuli. Further aspects of control that are gained through direct presentation include the ability to alternate between two or more odorants during a single session, presentation to one or both nostrils, presentation of "no odor" trials, and even the ability to manipulate the intensity of odor/concentration of odorant. In short, ambient odorant presentation limits experimenters to between subjects or block-wise manipulations, while direct odorant presentation allows for odor manipulations on a trial by trial basis.
Here the fundamentals of a method for testing OCDM using direct presentation of odorants with the aid of an olfactometer are presented15. An olfactometer is a machine that allows for the presentation of odorants at exact points in time (for example, contemporaneously with the onset of the presentation of a visual stimulus) and for a discrete amount of time (e.g., the presentation of a puff of air for 2 s). Furthermore, the olfactometer allows for the presentation to be directed below the nostrils, directly in one nostril, or directly in both nostrils. Olfactometers have long been utilized in memory research16,17. This protocol builds on previous research and applies it to the area of OCDM research.
All data collection in the original experiment15 was performed in accordance with the ethical guidelines of the American Psychological Association as well as the World Medical Association’s Declaration of Helsinki. The experiment was preapproved by the local Ethik-Kommission (equivalent to an Institutional Review Board). All subjects were made aware that their participation was voluntary and could at any time and without fear of penalty be terminated. All subjects signed informed consent.
1. Participant Recruitment and Pre-study Instructions
2. Experimental Design
NOTE: In the experiment outlined here (which corresponds to Experiment 1 from the original article15) the purpose was to determine whether the presence of an odor context during encoding and retrieval enhanced memory over a condition in which no extra odor context was present during both phases5. This is a variety of a CDM effect called context enhanced memory. The original experiment included more independent variables (odor valence and word valence) that are irrelevant for the current report. For details on the original experiment and specific information concerning the verbal material used, see the Supplementary Material from the original article15. The experiment is broken down into three different phases (See Table 1 for an overview).
Pre-study | Encoding phase | Retention interval | Retrieval phase |
1. Ensure pre-study instructions were follwed | 1. Present words one at a time | 1. 5 minute break in which subjects color in mandalas | 1. Present words one at a time |
2. Have subjects sign informed-concsent | 2. Subjects complete abstract/concrete categorization task | 2. Subjects complete old/new recognition test | |
3. Situate subjects in experimental room | 3. Present odorants on each trial | 3. Present odorants on each trial | |
4. Perform practice inhalation trials |
Table 1: Overview of the experimental procedure.
3. Stimulus Selection
One of the main purposes of the current experiment was to determine whether OCDM effects could be found when the olfactory context was presented directly, rather than ambiently. There were three main dependent variables (in line with common signal detection theory analyses26): the proportion of hits, the proportion of false alarms, and a corrected accuracy score termed d'. Given the focus of interest here, the data from the two odor groups from the original experiment15 (positive and negative odor) are combined and compared to the no odor group. Collapsing the data across these two groups provides the purest test of olfactory context enhancement.
As can be seen in Table 2, the olfactory context groups outperformed the no odor group in accuracy, by displaying more hits and significantly fewer false alarms as well as significantly higher d'. This is clear evidence that direct presentation of odorants can also lead to OCDM effects, as has been previously found for ambient presentation4,5.
This finding is somewhat surprising, given that previous experiments have shown odors to be poorer cues of memory in paired-associates tests (where odors are presented in the foreground)12,13 and notions that olfaction is an implicit sense11. Future research will be needed to determine what distinguishes using odors as paired-associates from using odors as contextual mnemonic cues.
n | d’ | Hits | False Alarms | ||
Control (no odor) | 20 | 1.54 (1.62) | .67 (.25) | .25 (.25) | |
Olfactory context | 40 | 2.18 (.50) | .75 (.13) | .13 (.05) | |
t | 2.29 | 1.57 | 2.90 | ||
p | .026 | .123 | .005 | ||
Cohen’s d | .53 | .40 | .67 |
Table 2: Means, significance test values, and effect sizes for comparisons between the control and olfactory context groups. Values in parentheses represent standard deviations.
The method described here, in which an olfactometer is used to directly present odorants as contextual stimuli, represents an expansion of the utility of olfactometers in olfactory memory research16,17. Specifically, this method allows for an expansion of the area of OCDM research. Previous research had shown that odors are indeed effective contextual mnemonic cues4,14, but all research to this point has utilized ambient presentation of odors. By using the method described here, it was shown that OCDM effects can also be found when odorants are presented directly, by means of an olfactometer15.
This methodology, with appropriate modifications, provides several benefits over ambient presentation. For one, direct presentation allows for presentation of odorants at specific times. This can help researchers answer several questions, such as determining whether an odor must be present contemporaneously with target material in order to be bound together, and eventually act as an effective contextual mnemonic cue. Another benefit is that direct presentation allows for trial by trial manipulations of odorant presentation. This can help researchers learn whether odors function similarly to other stimuli, which can be effective cues when altered rapidly between trials27. Other benefits include 1) allowing for presentation to a single nostril on one trial, 2) allowing for the presentation of multiple odorants on a single trial, and 3) allowing for the presentation of different intensities across trials. This list of the benefits of this methodology is not exhaustive but highlights its potential utility to future researchers.
Another potential benefit of using an olfactometer in OCDM research is that direct presentation may be less susceptible to adaptation and habituation than ambient presentation of odorants. Past OCDM research, which has exclusively utilized ambient presentation, has frequently made use of short encoding phases and long retention intervals, potentially to avoid problems of adaptation and habituation14. Any procedure that would allow for longer encoding phases and shorter retention intervals could have large practical benefits for future research in terms of allowing for more encoding phase manipulations and making organization of subjects easier. Future research is needed to investigate whether direct presentation is, indeed, less susceptible to adaptation and habituation than ambient presentation.
The use of an olfactometer to directly present odorants also has several limitations. For one, directly presenting odorants to subjects increases the likelihood that olfaction is in the center of attention. Direct presentation is, therefore, not suited to OCDM research that attempts to investigate whether a subject must be consciously aware of the olfactory context for odors to serve as effective contextual mnemonic cues. Furthermore, given that odors are generally outside the focus of our awareness on a day to day basis, the direct presentation method probably provides less external validity than the ambient presentation method.
There are several issues that researchers should consider when determining which type of olfactometer to use or build and other issues that researchers should consider about their experiment, depending on the properties of the olfactometer they have. For example, the original experiment made use of a discrete presentation olfactometer with three separate channels15. This particular olfactometer had an estimated flow rate of 97.4 mL/s and the tubes that led from the odorant jar to the end just below the subject's nose was 4.3 m long. A discrete presentation olfactometer presents puffs of air at discrete times. This could potentially lead to issues related to tactile information, which need to be considered by the researcher when planning the experiment (see 2.1.4.4.2). The number of channels determines the number of different odorants that can be used in a single experiment. Some research questions may require a large number of odorants to be presented to a subject in a single experimental sitting, and researchers must therefore ensure that their olfactometer has the appropriate number of channels. One more issue to consider is the length of the tubes used in the olfactometer, which determine the delay between presentation trigger and actual delivery to the subject. Researchers should test to ensure that the timing is appropriate for their research question.
When a researcher investigating OCDM is deciding whether to utilize direct or ambient presentation of odors, we would suggest the following, based on the goals of the particular research project. Ambient odor presentation should generally be preferred when matters of ecological validity are of primary concern to the researcher. Direct presentation may be preferable when matters of experimental control are of primary importance. Specifically, direct presentation should be preferred when investigating topics such as a) the role of attention towards the olfactory context, b) inter-nasal differences, c) trial by trial manipulations of presented context, and d) differences in presentation time of olfactory context. Of course, this list is not exhaustive, and there may be other situations where direct presentation of olfactory context is preferable to ambient presentation.
The authors have nothing to disclose.
The authors have no acknowledgements.
Olfactometer | Burghart Messtechnik | OG001 | Discrete presentation olfactometer |
Odiferous material_Onion | Burghart Messtechnik | LA-13-00236 | Liquid used in olfactometer to produce onion odor |
Odiferous material_Peach | Burghart Messtechnik | LA-13-00245 | Liquid used in olfactometer to produce peach odor |
E-Prime 2.0 | Psychology Software Tools | Experiment control software |