This chapter will mainly focus on the olfactory system and theoretical discussions on how olfaction has been studied in relation to memory and learning.
Figure 3.1 Olfactory pathway (Professer Claffey, 2012).7 What is Olfactory
The olfactory system represents one of the oldest sensory modalities in the phologenetic history on mammals (Vokshoor, Amor 2011)8. Nevertheless the olfactory system remains in many ways the least understood of the sensory modalities. The olfactory system is the most thoroughly studied component of the chemosensory triad and processes information about identity, concentration and
7 http://mikeclaffey.com/psyc2/notes-other-senses.html
8 http://emedicine.medscape.com/article/835585-overview
quality of a wide range of chemical stimuli. (Castle,P.C; 51 Purves D, Augustine GJ, Fitzpatrick D, et al., 2011). These stimuli are named odorants and interact with the olfactory receptor neurons in the olfactory epithelium that lines the interior of the nose. Via chemical sensors the olfactory systems makes us able to detect food and it influences social- and sexual behaviour. The system is an extremely discriminative and sensitive chemosensory system, which makes human beings able to distinguish between a predicted high of 1000 to 4000 odours.
In terms of naming odour different terms are used as describe in above chapter. In this chapter the word scent is being replaces with odour since the term odour is better fitted in the olfactory discussion.
Odour is normally caused by one or more volatilized chemical compounds, generally at a very low concentration and stems from a substance, which is somehow volatile, i.e. a substance that easily can turn into a gas. This substance will send off molecules – odorants. That is why non-volatile materials’ like steel do not have an odour.
(Dowdey, Sarah. 2007). 9
Factors like temperature and humidity have a great effect on odour due to the increased molecular volatility. This explains why garbage smells stronger in the heat and wood musty after rain. Other odours that are dissolved in water or fat tend to have a more intense odorant.
An odour is activated when airborne molecules stimulate the olfactory receptor cells.
The perception of these odours begins with the inhalation and transportation of volatile aromas to the olfactory mucosa, which, are located bilaterally in the dorsal posterior region of the nasal cavity. (Hutchins, 2012 )
The olfactory mucosa (figure 3.1) consists of a layer of columnar epithelium, surrounding millions of olfactory neurons; these are the only neurons to communicate with the external environment and are undergoing constant replacement. (Hutchins,
9http://science.howstuffworks.com/environmental/life/human-biology/smell.htm
2012) Basal cells near the lamina propria are undergoing differentiation and develop into these neurons about every 5-8 weeks.
When an air born odour sweeps up through the nostrils, the molecules hit the olfactory epithelium – the centre of olfactory sensation. When an odour is sensed, is done by the help from the olfactory receptors cells, which are neurons with knob-shaped tips called dendrites. When an odorant stimulates a receptor cell, the cell sends an electrical impulse to the olfactory epithelium. (Dowdey, Sarah. "How Smell Works" 29 October 2007). The olfactory bulb has close access to the amygdala, which processes emotion and the hippocampus, which is responsible for associative learning. Thus, we see a tight wiring, odours would not trigger memories if it weren’t for conditioned response. This conditioned response is started when you first smell a new odour, this odour you link to an event, thing, a person or a moment. The brain forges a link between the odour and a memory, e.g. cinnamon with Christmas or lavender with a summer memory in the South of France. When you encounter the odour again, the link is created and ready to elicit a memory or a mood.
In everyday life, odours are often connected to contextual relationship to other events, such as Christmas, dinner, persons, etc. as mentioned above. Attention often focuses on how we feel or behave towards the events rather than on naming or identifying the odour (Olsson 2003). According to (Engen 1991) “ Olfaction is a primitive survival system serving the function of quickly categorising experiences with the chemistry of the environment without reasoning about them (…) Odours are named by function, what one does with them and in what context (…) Other means of encoding than language must be involved” (pp. 83-85)
The interest in psychology and olfactory is growing area, whereas conventionally research on vision and auditory has tended to dominate behavioural science and sensory marketing. Even though research, concentrating on these sensory fields continues, attention is now more and more being directed towards the olfactory modality and in particularly to psychological effect of the odour. (Chu,Simon 2000) Olfactory discoveries
The psychology of olfaction or aroma-chology has involved several different focuses, including a wide rang of topics. This could be the effect of odour on specific behaviours; examples could be interpersonal and consumer behaviour. Other focuses
are the odours ability to effect emotional- and psychological changes e.g. changes in mood and behaviour, and the influence of odour manipulation on cognitive memory.
(Chu,Simon 2000) The power of odours to vividly remind one of a particular past experience is particular interesting in olfaction and memory. One anecdote that is often mentioned in the literature stems from Marcel Proust (1922/1969) (Chu, Downes 2000) (p. 4). Proust was reminded of a childhood experience by the smell of a tea-soaked pastry. Marcel Proust’s experience formed the basis of what has been known as the Proust phenomenon i.e. the ability of odours spontaneously to cue autobiographical memories, which are often very emotional and often old.
This experienced called involuntary autobiographical memory is a subcomponent of memory that occurs when encounters in everyday life evoke recollections of the past without conscious effort, e.g. like if a passing smell of cinnamon suddenly reminds you of Christmas.
This phenomenon called the Proustean Phenomena is interesting when discussing the possibilities for using odour in a marketing sense. The ability for odour to recall memories that is more emotional than memories elicited by other sensory stimuli.
Today there is a positive support for this statement, since many scientists in a number of cross-modal laboratories and autobiographical studies have conducted episodic memory studies comparing olfactory, visual, verbal, tactile and auditory variants of same cues. One study by Hertz and colleagues (1998) has consistently shown that when a cue is presented in olfactory form, memories are more emotional as indicated by self-report and physiological responses. Such as heightened heart rate compared to memories evoked by the same cue presented in other sensory formats (Herts et all 2003). Here, other studies have also shown that odour-cued memories were rated more pleasant than visual or verbal variants of same items.
Evidence for these findings can be explained via the olfactory systems location in the limbic system (figure 3.2), which is a cluster of brain structure including the hippocampus, amygdala, anterior thalamic nuclei, septum, limbic cortex and fornix,
which also is home for emotions, behaviour, motivation and long-term memory (Medline Plus 2012). 10
Figure 3.2 Limbic system11
Evidence supporting the emotional silence of odour-evoked recall have been shown by Herz et all 2003, who proved the emotional potency of odour –evoked memories via functional magnetic resonance imaging (fMRI). fMRI is an MRI procedure that measures brain activity by detecting associated changes in blood flow. The primary form of fMRI uses the blood-oxygen-level-dependent (BOLD) contrast. (figure 3.3) The study compared regions of activation during recall, triggered by olfactory and visual cues that were connected to meaningful memory and a comparable control cue presented in olfactory and visual form. The fMRI analyses indicated significantly greater activation in the amygdala and hippocampal regions during recall to the personally significant odour than other cue, and the behavioural responses confirmed that emotional responses were greater to the personally meaningful odour. These findings are providing a convincing neurobiological evidence for subjective experience of emotional potency of odour-evoked memory is correlated with activation in the amygdala. (Herz et al, 2003)
10 http://www.nlm.nih.gov/medlineplus/ency/imagepages/19244.htm
11 http://mycozynook.com/102RGCh28OH.htm
Figure 3.3 (Herz et al, 2003) displays the medial temporal lobe cluster of positive activation for the contrast between Experimental Odour (EO) and Experimental visual (EV) + Control odour (CO) +control visual (CV). As can be seen, significantly greater activation occurred in the amygdala for EO compared to the other cue types. (Hertz et al. 2003)
The positive activation difference for the comparison EO vs. EV + CO + CV is shown in color on the left side of the brain with the scale bar to the right in arbitrary MR units. The slice shown is at Z = −16 mm inferior to anterior commissure (AC). The maximum intensity difference of 1.65 (MR units) appeared at 14, 8, −16, relative to the AC, corresponding to left hemisphere Broadmann’s areas 28 and 34. The white outline denotes the regions of interest (ROI) on the left, including the hippocampus, amygdala, and parahippocampal gyrus, used for tests of lateralization
Generally, studies of the neurological functions of involuntary memory have been few. One study of the involuntary memory compared the involuntary memories with voluntary memories by using Positron Emission Tomography (PET). The study found that involuntary memory retrieval is mediated by the hippocampus, which is associated with episodic memory retrieval (Rugg, M.D, Fletcher, P. C. 1997).
One other study found that the medial temporal lobe, the posterior gyrus, and the precunueus are activated during retrival success with or without executive control seen within right dorsolateral prefrontal cortex. (Hall, N, M., Gjedde A. & Kupers, R 2008)12 This tells us that involuntary memories are retrieved using the same system
as voluntary memory when retrieving perceptual information. (Hall, N, M., Gjedde A. & Kupers, R 2008)
Role of the amygdala
The amgydala, which is an almond-shaped cluster of neurons situated deep in the brain’s medial temporal lobe and lies beneath the primary olfactory cortex (Science Daily)13 has proved to be involved in the formation of memories and emotional experience, especially those associated with defence and fear (Murray, Elizabeth A., et. al. (2009).
In complex vertebrates, the amygdala performs primary roles in the formation and storage of memories associated with emotional events. Research indicates that, during fear conditioning, sensory stimuli reach the basolateral complexes of the amygdalae, particularly the lateral nuclei, where they form associations with memories of the stimuli. (Murray, Elizabeth A., et. al. (2009).
There are functional differences between the right and left amygdala. In one study, electrical stimulations of the right amygdala induced negative emotions, especially fear and sadness. In contrast, stimulation of the left amygdala was able to induce either pleasant or unpleasant.
Bilateral activation of the brain has been seen with experiments with unilateral stimulation, which can be accomplished by placing an odour stimulus under one nostril. Here we can se that the activation is not exactly equal in both hemispheres (Olsson, Mats 2003). The explanation is that different parts of the brain are involved in olfactory memory depending of what type of memory is being processed i.e.
implicit memory or explicit memory. Previous studies have shown that the left hemisphere is activated during verbal semantic retrieval of odour-related memories, where the right hemisphere proves activation during non-verbal retrieval of semantic odour-relate information. (Olsson, Mats 2003)
There are also direct projections to the hippocampus, which are involved in the integration of various sensations into memory. Neuropsychological researchers have suggested that this pathway is important for the development of olfactory memories.
13 http://www.sciencedaily.com/articles/a/amygdala.htm
The primary olfactory cortex has both direct and indirect pathways connected to the amgydala, which is vital for e.g. an animal or a human to create memories of olfactory stimuli, which can threaten the survival. (Olsson, Mats 2003)
Memories of Odours
Scientists and philosophers have long wondered how we manage to remember odours despite the fact that each olfactory neuron in the olfactory epithelium only survives for about 60 days where after new cells replace them. The replacement of neurons in the olfactory epithelium differs from most processes of the body, where neurons die without any successors (Pines, Maya)14. When olfactory neurons die, a layer of stem cells beneath them constantly generates new olfactory neurons to maintain a stable supply.
Recollection of memory
The relationship between odour naming (to reflect semantic memory) and odour recognition memory (to reflect episodic memory) has been the topic of considerable interest to investigators studying odour and flavour perception. Understanding this connection is important to the understanding of the fundamental processes underlying olfactory perception and cognition.
Previous studies of odour and memory have dealt primarily with explicit forms of memory, which is the conscious memory, i.e. recollection of previous experience and information we use throughout the day to remember appointments and memory of e.g. an event from years ago. (Bernard J. Baars and Nicole M. Gage 2010) Explicit memory or declarative memory involves conscious recollection where implicit memory is unconscious and unintentional form of memory, this memory is also characterised as long-term memory.
There are two types of explicit memory, one part called the episodic memory and one called the semantic memory. The episodic and the semantic memory combined forms the autobiographical memory system. (Bernard J. Baars and Nicole M. Gage 2010) The autobiographical memories consist of the recollection of events in a person’s life, like experience, people and particular time and place (episodic) and general knowledge like facts (semantic). These memories can be something that happened to
14 http://www.hhmi.org/senses/d140.html
the person directly or memories of events that happened around them. Episodic memory is necessary when remembering your past i.e. “time travelling”. (Bernard J.
Baars and Nicole M. Gage 2010) Semantic memories are knowledge of historical events, mathematics, writing and reading or recognition of friends.
A study of autobiographical memory conducted by Johan Willander and Maria Larsson (2007), investigated the influence of verbal and conceptual processing on the retrieval and phenomenological evaluation of olfactory evoked memories, and whether the experienced qualities of retrieved information are affected by olfactory exposure per se. (Willander,Johan 2007)
The test subjects whom were all older adults were randomized into one of three cued conditions (odour only, name only or odour name) and then asked to relate to any autobiographical event for the given cue.
The main aim of the study was to explore whether (1) the age distribution of olfactory-evoked memories differs from memories cued by words and pictures and (2) the experimental qualities of the evoked memories vary over the different cues.
The result showed that autobiographical memories triggered by olfactory information were older than memories associated with verbal and visual information. Specifically, most of the odour-cued memories were located to the first decade of life <10 years, whereas memories associated with verbal and visual cues peaked in early adulthood
<11-20 years. Interestingly, odour-evoked memories also were associated with stronger feelings of being brought back in time and these memories were less thought of, compared with memories evoked by verbal and visual information. The findings and pattern from the study may suggest that odour-evoked memories may be different from other memory experiences. (Willander,Johan 2007)
Figure 3.4 Autobiographical odour memory page 1661 (Willander,Johan 2007)
If looking at the diagram A in figure 3.4 we see that 40% of odour–only evoked memories were dated back to the childhood (0-10 years old) and 20% from childhood
& early adulthood (11 – 20 years old). In diagram B the proportion of memories
AUTOBIOGRAPHICAL ODOR MEMORY 1661 The Distribution of Memories Over
the Life Span
For each participant, the number of evoked memories dated to a specific decade was divided by the subject’s total number of memories. The proportions were then submitted to a mixed two-way ANOVA with cue type as between-groups factor, and decade as within-group factor. The analysis yielded a main effect of decade [F(7,63) 12.18, p .001]. Post hoc testing showed that a higher proportion of memories were located to the first two decades as com-pared to the third to eight decades. Also, more memories were overall localized to the first than to the second decade.
Interestingly, the interaction between cue type and decade was significant [F(14,126) 1.76, p .05]. The source of this interaction was related to the first decade where more memories were generated in the odor-only condition as compared to the name-only condition. The amount of memories generated in the odor-name and odor-only con-ditions, and odor-name and name-only conditions did not differ reliably (ps .05). No other comparisons were reli-able. The age distributions across the three cue conditions are displayed in Figure 1. Given the unbalanced number of men and women across the three conditions meaningful gender analyses could not be performed.
Experiential Ratings
The experiential data for the evoked memories across the two conditions (rating with the cue/rating without the cue) were submitted to a 3 (cue type) r 2 (rating condi-tion) mixed ANOVA. The first factor varied between sub-jects and the second within subsub-jects.
The ANOVA on rated pleasantness (valence) revealed a main effect of cue type [F(2,69) 5.18, p .01]. Tukey post hoc analysis indicated that odor-only evoked memories (M 6.43, SD 1.74) were rated as more pleasant than the name-only evoked memories (M 5.49, SD 1.38). The memories evoked by odor names (M 5.97, SD 1.11) did not differ from odor-only or name-only evoked memories on rated pleasantness. The main effect of rating condition was not significant (p .70). No interaction effect between cue type and rating condition was observed (p .30).
A main effect of cue type was demonstrated for emo-tionality [F(2,69) 3.59, p .05]. Tukey post hoc com-parisons indicated that memories evoked in the odor-only condition were more emotional (M 5.22, SD 2.00) as compared to the name-only (M 4.01, SD 1.54) and odor-name (M 4.23, SD 1.80) conditions. The name-only and odor-name conditions did not differ reliably. No main effect of rating condition was observed (p .20).
The interaction between cue type and rating condition was not significant (ps .90).
Cue type had a reliable effect on the feeling of being brought back in time to the occurrence of the event [F(2,69) 4.30, p .05]. The odor-only evoked memo-ries (M 6.66, SD 1.39) were experienced with a stron-ger feeling of being brought back in time as compared with memories evoked by name-only (M 5.68, SD 1.28) or odor-name cues (M 5.91, SD 1.61). Ratings in the name-only and odor-name conditions did not
dif-A
Proportion of Memories
Age at Event (years)
0–10 11–20 21–30 31–40 41–50 51–60 61–70 71–80 0
.1 .2 .3 .4 .5
B
Proportion of Memories
Age at Event (years) 0
.1 .2 .3 .4 .5
C
Proportion of Memories
Age at Event (years) 0
.1 .2 .3 .4 .5
0–10 11–20 21–30 31–40 41–50 51–60 61–70 71–80
0–10 11–20 21–30 31–40 41–50 51–60 61–70 71–80
Figure 1. The distribution of (A) odor-only-, (B) name-only-, and (C) odor-name-evoked autobiographical memories across the life span. Error bars indicate 1 standard error.
evoked by name-only are significantly lower with different age proportions. Here, approximately 15 to 20% of the memory proportions stems from the age (10- 20 years old). The odour-only evoked memories in A were experienced with stronger feelings of being brought back in time as compared with memories evoked by name-only in B.
This may indicate that the age distribution, the phenomenological qualities and the number of evoked memories are affected by explicit knowledge of the provided odour cue. This suggests that conceptual processes may have a significant influence on the retrieval of autobiographical olfactory information. In fact, knowledge of an odour’s name resulted in a distribution taking an intermediate position in diagram C, and thereby not being statistically different from the age distributions obtained for the name-only and the odour-only cued condition. The observations suggest that olfactory knowledge creates a shift from perceptual to more conceptually driven retrieval process in the context of different types of sensory cues and evokes different types of retrieval processes.
The overall result of the study supports the concept that olfactory evoked memories are more emotional than memories evoked by verbal cues and the age where the memories tend to cluster. This result is interesting in further discussion in this study.
The knowledge of the proportions of memories in the early childhood could be important when discussing odour in connection to branding.
Explicit and implicit memory
In olfactory, explicit memory is about making associative meaning to odour (Olsson, Mats 2003). Previous studies of odour memory have, according to Mats Olsson (2003), dealt with explicit forms of memory even though implicit forms of memory may provide a common means to learn about odours.
In the context of the relationship between awareness and memory, Graf and Schacter (1985) made an important distinction between implicit and explicit memory tasks. In tasks concerning explicit memory (e.g. recall, recognition), test instructions are directed toward conscious recollection of a prior event or study episode. In contrast, in implicit memory tasks (e.g. perceptual identification, fragment completion, stem completion), no reference is given to a prior learning episode; participants are not informed of the connection between the study and the test.
Explicit memory of odour can be used to process information and compare encountered odours. Evidence of explicit olfactory memory is seen through behaviours in tasks that evolved a working memory component (Olsson, Mats 2003).
Previously common tests, used in explicit odour memory, are odour identification and odour recognition. Here odour recognition is the most used and direct means to measure odour memory.
One of the most common and direct means used to measure odour memory, is odour recognition. (Wilson, Donald A. and Stevenson, Richard J. 2003) In this kind of odour recognition test participants are asked whether or not they recognize an odour.
The participant is subjected to a certain olfactory-related stimulus and after an interruption period asked to decide if a probe, i.e. a stimulus, - could be the same as the initial stimulus, if this one is the same as the participant initially encountered.
(Wilson, Donald A. and Stevenson, Richard J. 2003). Ways of testing the effect of verbal labelling could include comparisons of odour and odour name and the speed and accuracy of which lexical decision that was used for naming the odour. (Wilson, Donald A. and Stevenson, Richard J. 2003)
Unlike odour recognition, odour identification, which is another way of testing odour memory, requires the specific labelling of the present olfactory stimuli. According to a study (Wilson, Stevenson 2006) the ability of humans verbally identification of odours is very restricted despite the ability to differentiate hundreds of odours.
A study conducted by Wilson, Stevenson (2006) on synthetic olfactory perception suggests two types of findings. The first finding derives from experiments in which participants were asked to identify component parts of odour mixtures, where the participants first had learned the labels for each of the odorants to be mixed. The participants were presented with mixtures consisting of two or more constituents. The test showed that participants rarely could identify an individual odour while being presented in a mixture consisting of three or more components. In summery, the study suggested that olfactory processing mainly is synthetic at the behavioural level.
Context dependent and autobiographical memory
Context-dependent memory is the memory-effect whereby retrieving information in the same environment in which it was encoded (in contrast to autobiographical memory). This method is said to lead to better memory performance than e.g.
encoding and retrieving in different context.(Chu, Downes 2000).
Researchers like Hertz (1997) found that ambient odour functions are effectively in environmental context, in context-dependent memory studies.
One example to demonstrate the context-dependent memory is e.g. if an item is lost like a key, typically people try to systematically retrace their steps to determine all the possible places, where the key might be located. Often, when back at the location where the key is lost, your memory of where the key is, is retrieved.
Hertz (1997) suggested that odours, which were out of place in the experiment situation, were associated with best memory performance when reinstated at retrieval.
Implications of these findings are ambient odours at the time of an event can be encoded along with event details and afterwards be used as cues in the retrieval of those event details. This information is interesting in the context of autobiographical memory research as well. However the kind of memories most commonly reported in Proustian memory are those, which are especially old, vivid and emotional.
One of the first examinations of odour-evoked memory conducted by Herz and Cupchik (1995) (Hertz, Rachel S. and Engen, Trygg 1996) used the method of paired-associated incidental learning paradigm to examine whether odours evoked more emotionally memories than verbal cues. In the experiments 16 emotionally evocation paintings were paired with 16 cues, either odours or verbal odour labels. The recall of the painting was conducted 48 hours later by a cued recall.
The result of the experiments showed that the response was equivalent between the two cues. Besides these findings, another interesting result was experienced in the same test. It showed that when a painting was recalled to an odour, there were more emotion elicited in the recollection, more emotions experienced, higher emotional intensity and greater confidence in emotional memory compared to recall associated to verbal cues.