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Olfactory memory refers to the recollection of odours. Studies have found various characteristics of common memories of odour memory including persistence and high resistance to interference. Explicit memory is typically the form focused on in the studies of olfactory memory, though implicit forms of memory certainly supply distinct contributions to the understanding of odours and memories of them. Research has demonstrated that the changes to the olfactory bulb and main olfactory system following birth are extremely important and influential for maternal behavior. Mammalian olfactory cues play an important role in the coordination of the mother infant bond, and the following normal development of the offspring. Maternal breast odors are individually distinctive, and provide a basis for recognition of the mother by her offspring.

Olfactory memory was developed throughout evolution for a number of various reasons. Among the most notable reasons are those related to the survival of the species and the development of early communication. Even in humans and animals today, these survival and communication aspects are still functioning. There is also evidence suggesting that there are deficits in olfactory memory in individuals with brain degenerative diseases such as Alzheimer's disease and dementia. These individuals lose the ability to distinguish smells as their disease worsens. There is also research showing that deficits in olfactory memory can act as a base in assessing certain types of mental disorders such as depression as each mental disorder has its own distinct pattern of olfactory deficits.

How does olfactory memory occur?Edit

PhysiologyEdit

OdorantEdit

An odorant is a physiochemical molecule that binds to a specific receptor protein.[1] In mammals, each olfactory receptor protein has one type of molecule that it responds to, known as the one-olfactory-one-neuron rule, and approximately one thousand kinds of which have been identified.[2] Structure and complexity constitute an odorant’s features, with changes resulting in altered odorant quality.[1] An odorant’s features are detected by the olfactory system’s glomeruli and mitral cells which can be found in the olfactory bulb, a cortical structure involved in the perceptual differentiation of odorants.[1][3] The olfactory bulb itself affects how odours come to be encoded through its temporal structure and firing rate, which in turn influences the likelihood of an odorant being remembered.[1]

NeuromodulatorsEdit

Neuromodulation exists in the olfactory system and is responsible for neural plasticity and behavioural change in both mammals and insects.[4] In the context of olfactory memory, neuromodulators regulate storage of information in a way that maintains the significance of the olfactory experience.[4] These systems are highly dependent on norepinephrine and acetylcholine, which affect both implicit and explicit memory.[4] Studies involving the noradrenergic system of mice demonstrate elimination of habitual learning when areas involving this system are lesioned, and subsequent restoration of habitual learning abilities when noradrenaline is injected into the olfactory bulb.[5] The importance of cholinergic systems has been demonstrated in studies of rats and the effects of scopolamine, with acetylcholine being involved in initial learning stages and more specifically in the reduction of interference between stored memories.[6]

Implicit odour memoryEdit

Implicit memories of stimuli do not require conscious recollection of the initial encounter of the stimulus.[7] In regards to olfactory memory, deliberate recollection of an odour experience is not necessary in order for implicit memories of odours to form in the brain.[7] Techniques used to study implicit olfactory memory are considered to be applicable to both humans and animals.[8] In tests of implicit memory, memory of a stimulus is shown to be aided by previous exposure to that same stimulus.[8] Evidence of the formation of implicit memory is found in tests of habituation, sensitization, perceptual learning and classical conditioning.[4] In olfaction there exists a strong tendency for habituation, which is discussed further in the following paragraph.[7] By evaluating memory performance of tasks involving one of these ‘subsets’ of implicit memory, the effect of previous odour stimulus experience not involving conscious recollection can be measured.[9] Further knowledge can be gained about implicit memory of odour through the study of the implications of cognitive deficits. The effects of brain injury on odour memory can be investigated through the use of thee implicit memory measures leading to further overall understanding of the brain.[9]

HabituationEdit

Habituation involves decreased levels of attention and responsiveness to a stimulus that is no longer perceived as being novel.[7] In the realm of olfactory memory, habituation refers to a decrease in responsiveness to an odour as a result of prolonged exposure (restricted to a certain repeated stimulus), which involves adaptation of cells in the olfactory system.[4] Receptor neurons and mitral cells located in the olfactory system adapt in response to odours.[4] This includes the involvement of piriform cortical neurons which adapt rapidly, more completely and selectively to novel odours and are also thought to play a very important role in the habituation of odours.[4] Norepinephrine is considered to have an effect on the functioning of the mitral cells by increasing their responsiveness.[4] Acetylcholine is also regarded as an important neurotransmitter involved in the habituation of olfactory stimulus, though the exact means through which it operates are not yet clear.

Explicit memoryEdit

Explicit, unlike implicit memory for odours, is thought by some to be a phenomenon that is exclusive to humans.[8] Explicit memory refers to memories that are remembered with conscious awareness of doing so.[10] In olfaction, explicit memory refers to attributing associative meaning to odours.[4] Through the assignment of associations to odours as well as non-odour stimuli, olfactory stimuli can gain meaning.[4] Explicit memories of odours include information which can be used to process and compare other encountered odours.[4] Attention focused on odours aids in the functioning of everyday life as well as the engagement of proper responses to experienced events.[11] Evidence of explicit olfaction memory is seen through behaviours in tasks involving a working memory component.[4] The two most commonly used tests for explicit odour memory are odour identification and odour recognition, which are discussed in greater detail below.[9]

Odour recognitionEdit

Odour recognition is the most common and direct means used to measure odour memory.[8] In an odour recognition test participants are asked whether or not they recognize an odour. More specifically, a participant is subjected to a certain olfactory-related stimulus, and after a delay period is asked to decide if a probe (a stimulus that could or could not be the same as the initial stimulus) is the same as the one he/she initially encountered.[8] Memory accuracy is assessed by the amount of correct recognition decisions are made.[8] A potential problem with this measure involves the generation of verbal labels that may enhance memory for olfactory stimuli. There are various ways of measuring the effect of verbal labeling, which include comparison of odours and odour names, as well as the speed and accuracy with which lexical decisions are made regarding odour names.[9] It has been suggested that odour recognition testing should be considered as a measure that involves both memory for perceptual information as well as potentially confounding memory due to the generation of verbal labels.[9]

Odour identificationEdit

Odour identification requires the specific labeling of presented olfactory stimuli, unlike odour recognition.[8] The ability of humans to verbally identify odours is very restricted despite the ability to differentiate hundreds of odours.[9] It has been hypothesized that such poor odour identification performance is due to a weak link between odours and language.[8] However, it is possible that this poor connection is not due to limitations imposed by the human olfactory system, but by the way odours are gradually learned and because no formal education exists for the naming of odours as does for visually identifiable stimuli.[8] The difficulty in identifying and giving a label to olfactory stimuli is known as verbal-semantic processing, and is thought to grow increasingly worse with age, consequently affecting odour recognition.[9]

Hemispheric differencesEdit

Although bilateral activation of the brain has been seen with unilateral stimulation (accomplished by placing a stimulus under one nostril only), the activation seen is not exactly equal in both hemispheres.[11] Different parts of the brain are involved in olfactory memory, depending on what type of memory is being processed (e.g. implicit memory-habituation or explicit memory-recognition) and this is evident in the results of explicit and implicit tasks of memory.[11] Studies have shown that the left hemisphere is activated during verbal semantic retrieval of odour-related memories, while the right hemisphere shows activation during non-verbal retrieval of semantic odour-related information.[11] Much overlap does occur between regions, however.[4] Information of odours of a semantic nature is distributed across both sides of the brain, although the right hemisphere is more involved in the processing of odour quality and previous encounter of the stimulus than the left.[11] Neural plasticity is also an important part of olfaction, as different experiences may result in alterations of both cortical and subcortical circuitry in the brain.[4]

Role of the amygdalaEdit

The amygdala is a complex set of nuclei situated in the anterior temporal lobe and lies beneath the primary olfactory cortex. The amygdala is involved in the formation of memories of emotional experiences, particularly those associated with fear, flight, and defense. It is connected by various pathways to other parts of the brain, but most notably to the basal forebrain which contains magnocellular cells which provide extensive input into the neocortex and hippocampus. There are also direct projections to the hippocampus from the amygdala, which are involved in the integration of various sensations into memory. Neuropsychological research has suggested that this pathway is vital for the development of olfactory memories. The primary olfactory cortex and the hippocampus have extensive connections with the amydgala through both indirect and direct pathways. It is important for an animal to create memories of olfactory stimuli which threaten its survival. Without a properly functioning amygdala, olfactory memories would not be able to form which could put an animal or risk of dangerous stimuli in its environment due its lack of memory of such stimuli.[12]

Behavioural effectsEdit

Neurological and structural developmentEdit

Studies demonstrate that the changes to the olfactory bulb and main olfactory system following birth are extremely important and influential for maternal behavior.[13] Pregnancy and parturition result in a high state of plasticity of the olfactory system that may facilitate olfactory learning within the mother.[14] Neurogenesis likely facilitates the formation of olfactory memory in the mother, as well as the infant.[14] A significant change takes place in the regulation of olfaction just after birth so that odours related with the offspring are no longer aversive, allowing the female to positively respond to her babies.[14] Research with a variety of animals suggest the role of norepinephrine in olfactory learning, in which norepinephrine neurons in the locus cerulus send projections to neurons in the main and accessory olfactory bulbs.[15] This is significant in the formation of olfactory memory and learning.

The main olfactory bulb is one of the neural structures that experiences profound change when exposed to offspring odours at the time of childbirth.[14] Human neuroimaging studies suggest that activation of the medical prefrontal cortex (mPFC) occurs during tests of olfactory memory.[16] The medial prefrontal cortex receives extensive olfactory projections, which are activated immediately after birth in correspondence with primary olfactory processing regions.[16] Although there is no functional specificity for the main or accessory olfactory systems in the development of maternal behaviors, it has been shown that the main olfactory system is affected when individual odour discrimination of the offspring is required; this system experiences significant change following exposure to offspring odours after giving birth.[14] Changes in synaptic circuitry also contribute to the level of maternal responsiveness and memorization to these odours.[14]

Olfactory cuesEdit

Mammalian studiesEdit

Mammalian olfactory cues play an important role in the coordination of the mother infant bond, and the following normal development of the offspring.[14] The offspring of several different mammals are attracted to the odour of amniotic fluid, which helps to calm and adapt the infant to the novel environment outside of the womb.[17] in olfactory imprinting in sheep ewes form olfactory recognition memory for their lambs within 2–4 hours of giving birth, which causes the mother to subsequently reject advances from unfamiliar lambs and scents.[16] This bond is thought to be enhanced by olfactory cues that cause enhanced transmission across synapses of the olfactory bulb.[16] After the birth of the offspring, there is a shift in the value of the infant’s odours to the mother, which causes change in neural structures such as the olfactory bulb.[14] These changes contribute to maternal responsiveness and memorization of these odours.[14] Olfactory cues from the baby lamb are important in establishing maternal behavior and bonding. After birth, the smell of amniotic fluid (which was previously disgusting) becomes attractive for ewes.[13]

Amniotic fluid is one of the primary olfactory cues that the ewe is exposed to after birth, allow her to be attracted to any newborn lamb associated with that amniotic fluid.[14] The amniotic fluid produces olfactory cues, and a response from the ewe that cause her to be attracted to the newborn lamb.[14] When newborn lambs were washed with soap (or even water) it greatly reduced the degree of licking behavior by the maternal ewe, and consequently prevented her from displaying acceptance behavior towards the newborn.[14] The main olfactory system in sheep is quite significant in the developing appropriate maternal behaviors in sheep.[13]

Physiological, behavioral and anatomical evidence show that some species may have a functioning olfactory system in utero.[17] Newborn infants respond positively to the smell of their own amniotic fluid, which may serve as evidence for intrauterine olfactory learning.[17] Mammals’ sense of smell becomes mature at an early stage of development.[17] Fetal olfactory memory has been demonstrated in rats, for example. This is shown by rat pups, who avoid odours that they experienced in association with a noxious stimulus prior to birth.[15] While animal studies play an important role in helping discover and learn olfaction memory of humans, it is important to pay attention to the specifics of each study, as they cannot always be generalized across all species.[14]

Human studiesEdit

Research studies provide evidence that the fetus becomes familiar with chemical cues in the intrauterine environment.[17] Intrauterine olfactory learning may be demonstrated by behavioral evidence that newborn infants respond positively to the smell of their own amniotic fluid.[17] Infants are responsive to the olfactory cues associated with maternal breast odours.[15] They are able to recognize and react favorably to scents emitted from their owns mother’s breasts, despite the fact that they also may be attracted to breast odours from unfamiliar nursing females in a different context.[15] The unique scent of the mother (to the infant) is referred to as her olfactory signature.[15] While breasts are a source of the unique olfactory cue of the mother, infants are also able to recognize and respond with familiarity and preference to their mother’s underarm scent.[15]

Olfactory cues are widespread within parental care to assist in the dynamic of the mother-infant relationship, and later development of the offspring.[14] In support of fetal olfactory learning, newborn infants display behavioral attraction to the odour of amniotic fluid.[15] For example, babies would more often suck from a breast treated with an amount of their own amniotic fluid, rather than the alternative untreated breast.[15] Newborns are initially attracted to their own amniotic fluid because that odour is familiar. Although exposure to amniotic fluid is eliminated after birth, breast fed babies have continued contact with cues from the mother’s nipple and areola area. This causes breast odours to become more familiar and attractive, while amniotic fluid loses its positive value.[15] Maternal breast odours are individually distinctive, and provide a basis for recognition of the mother by her offspring.[15]

Role of olfaction in maternal bonding and subsequent developmentEdit

As demonstrated by animals in the wild (the great apes, for example), the offspring is held by the mother immediately after birth without cleaning and is continually exposed to the familiar odour of the amniotic fluid (making the transition from the intrauterine to extrauterine environment less overwhelming).[17] In newborn mammals, the nipple area of the mother is significant as the sole source of necessary nutrients.[15] The maternal olfactory scent that is unique to the mother becomes associated with food intake, and newborns who do not gain access to the mother’s breasts would die shortly after birth.[15] As a result, it seems natural selection should favor the development of a means to help in maintain and establish effective breast feeding.[15] Maternal breast odours signal the presence of a food source for the newborn.[17] These breast odours bring forth positive responses in neonates from as young as 1 hour or less through to several weeks postpartum.[15] The mother’s olfactory signature is experienced with reinforcing stumuli such as food, warmth and tactile stimulation; enhancing further learning of that cue.[15]

While infants are generally attracted to the odours produced by lactating women, infants are particularly responsive to their mother’s unique scent.[15] These olfactory cues are used in mammals during maternal care for coordination of mother-infant interaction.[14] Familiarization with odours that will be encountered after birth may help the baby adapt to the otherwise unfamiliar environment.[17] Neural structures such as the olfactory bulb undergo extensive changes when exposed to infantile odours; providing a starting point for individual recognition by the mother.[14] Odours from the breasts of lactating women serve as attractants for neonates, regardless of feeding history of the infant.[15] Maternal olfactory learning occurs due to the high state of plasticity and flux within the olfactory system during pregnancy and parturition.[14]

EvolutionEdit

Search for foodEdit

Studies of the mammalian brain have discovered that the excess of cerebral neurons is a phenomenon of mainly animals which had to seek and capture food. These neurons have become a large part of the olfactory system throughout evolution to allow higher mammals such as primates to have a better chance for survival through more advanced methods of hunting and finding food.[18] For example, the vulture has a large part of its brain committed to olfactory senses. This allows for it to be able to detect food at long ranges without being able to see it.[19] Having memory for various types of food aids in survival by allowing the animals to remember which scent it edible and which is not.

Communication and identificationEdit

Olfactory memory has also been developed throughout evolution to help animals recognize other animals.[20] It is suggested that smell allows for young infants to identify with their mothers or for humans to identify between males and females.[20] Olfaction cues were also used, and are still used, by many animals to mark territory, protecting themselves from other threats to their survival.[21] While the development of other sensory systems, such as the visual and auditory systems, has decreased how reliant some animals are on the olfactory system, these is still evidence that shows these animals’ olfactory systems still have a strong influence on their social interactions.[22] The memory for specific odorants gives the animal an opportunity to communicate with members of the same species and allows for lack of communication between species that do not have the proper receptor systems for the odour.[22] These chemical signals can also be sensed in the dark or even under water.[22]

Sexual reproductionEdit

Olfaction is a very important aspect in sexual reproduction throughout evolution because it triggers mating behaviour in many species.[21] Pheromones as olfactory chemical signals allow for members of the same species to perceive when other members are ready for reproduction.[22] It can also lead to the synchronization of menstrual cycles in females within the species and influence sexual attraction between members within the species.[22] Having an unconscious memory for such processes has allowed for species, and humans, to survive.

Warning stimulusEdit

The development of a sense of smell is also thought to have arisen to function as an arousal system. Once an odour enters into conscious memory, it can signal the presence of a threat, like the smell of gas or smoke. However, odour memory can also be an implicit or unconscious process. This ability to respond automatically to a warning stimulus is much like pre-attentive processes in other sensory systems which involve the use of automatic forms of memory. These response patterns have evolved over time and involve a wide variety of motor and autonomic responses which are integrated into the behaviour pattern of reacting to a warning stimulus. Odour-induced anxiety can be caused when an animal senses a predator. A study conducted on rats showed that when a rat was exposed to cat odours, there was increased anxiety-related behaviour in the rat. The cat odour induced an inhibition of the endocannabinoid system in the amygdala which has been suggested to induce anxiety-related responses.

Olfactory memory deficitsEdit

Olfactory deficits in the brainEdit

Olfactory memory deficits can be significant indications of a number of things going on within the brain. There is evidence to suggest that certain mental disorders produce olfactory deficits and olfactory deficits can in turn be a significant predictor of mental disorders. An example of two mental disorders that have significant deficits in olfactory memory are Alzheimer’s disease and Dementia. Some other olfactory deficits have been discovered in vascular dementia, dementia with Lewy bodies, Parkinson’s disease, and Huntington’s disease.[23] There is also evidence to suggest that certain brain altering drugs such as anti-depressants produce deficits in olfactory memory.[24]

Olfaction deficits and testingEdit

Many tests have been developed to test olfactory memory in patients with mental disorders such as the Brief Smell Identification Test where participants with dementia underwent a twelve part smell identification test which found that as dementia worsens so does the ability to distinguish smells.[23] In testing the effects of anti-depressants on olfactory sensitivity in mice, the “mice were tested in a Y-maze with a choice between an odourant (butanol) or distilled water before and during 3 weeks of dailyintra-peritoneal injection of either citalopram or clomipramine. Their performance was compared with those of a control group injected with a saline solution”[24] and the results were that significant olfactory deficits were found during the three week period of testing.[24]

Olfaction deficits and prediction of mental illness or diseaseEdit

Olfactory deficits have been found in patients suffering from mental disorders and there is evidence suggesting that olfactory deficits can be a predictor of mental illness and disease. Research suggests that olfactory memory deficits can be good predictors of several mental disorders such as depression, dementia and neurodegenerative disease, as each disorder has its own distinct features leading to specific predictions about what type of mental disorder a person may have.[25]

See alsoEdit

ReferencesEdit

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  2. Pinel, J.P. (2006). Biopsychology. 6th ed. Boston, MA, US: Pearson Education Inc.
  3. Guerin, D. (2008). Noradrenergic neuromodulation in the olfactory bulb modulates odour habituation and spontaneous discrimination. Behavioral neuroscience, 122(4), 816.
  4. 4.00 4.01 4.02 4.03 4.04 4.05 4.06 4.07 4.08 4.09 4.10 4.11 4.12 4.13 Wilson, DA. (2006). Learning to smell: Olfactory perception from neurobiology to behavior.. Baltimore, MD, US: Johns Hopkins University Press.
  5. Guerin, D. (2008). Noradrenergic neuromodulation in the olfactory bulb modulates odour habituation and spontaneous discrimination. Behavioral neuroscience, 122(4), 824.
  6. De Rosa, Eve. (2000). Muscarinic Cholinergic Neuromodulation Reduces Proactive Interference Between Stored Odor Memories During Associative Learning in Rats. Beahvioural Neuroscience, 114(1), 29-40.
  7. 7.0 7.1 7.2 7.3 Rouby, C., Schaal, B., Dubois, D., Gervais, R., & Holley, A., (Eds.). (2002). Olfaction, taste and cognition. New York: Cambridge University Press.
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  10. Radvansky, G., (2006). Human Memory. Boston, MA: Pearson Education Group, Inc.
  11. 11.0 11.1 11.2 11.3 11.4 Olsson, MJ. (2003). Implicit and explicit memory for odors: Hemispheric differences. Memory & cognition, 31(1), 44-50.
  12. Buchanan, TW. (2003). A specific role for the human amygdala in olfactory memory. Learning & memory, 10(5), P 319.
  13. 13.0 13.1 13.2 Lévy, F., Locatelli, A., Piketty, V., Tillet, Y., & Poindron, P. (1994). Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and miltiparous ewes. Physiology and Behavior (57) 1: 97-104.
  14. 14.00 14.01 14.02 14.03 14.04 14.05 14.06 14.07 14.08 14.09 14.10 14.11 14.12 14.13 14.14 14.15 14.16 Lévy, F., Keller, M., & Poindron, P. (2003) Olfactory regulation of maternal behavior in mammals. Hormones and Behavior 46: 284-302.
  15. 15.00 15.01 15.02 15.03 15.04 15.05 15.06 15.07 15.08 15.09 15.10 15.11 15.12 15.13 15.14 15.15 15.16 Porter, R.H., Winberg, J. (1997). Unique salience of maternal breast odors for newborn infants. Neuroscience and Biobehavioral Reviews 23: 439-449.
  16. 16.0 16.1 16.2 16.3 Broad, K.D., Hinton, M.R., Keverne, B., & Kendrick, K.M. (2002). Involvement of the medial prefrontal cortex in mediating behavioral responses to odor cues rather than olfactory recognition memory. Neuroscience (114) 5: 715-729.
  17. 17.0 17.1 17.2 17.3 17.4 17.5 17.6 17.7 17.8 Varendi, H., Christensson, K., Porter, H., Winberg, J. (1997). Soothing effect of amniotic fluid smell in newborn infants. Early Human Development 51: 47-55.
  18. Magill, Frank Northern. 1998. Psychology Basics. Pasadena, CA: Salem Press. P 418-419.
  19. Gazzaniga, Michael S. 1998. The Mind’s Past. Berkeley, CA: University of California Press. P 105.
  20. 20.0 20.1 Goldstein, Bruce E. 2002. Sensation and Perception: 6th Edition. Pacific Grove CA: Wadsworth Group. P 477.
  21. 21.0 21.1 Goldstein, Bruce E. 2002. Sensation and Perception: 6th Edition. Pacific Grove CA: Wadsworth Group. P 475.
  22. 22.0 22.1 22.2 22.3 22.4 Stockhorst, Ursula &Pietrowsky, Reinhard. 2004. Olfactory perception, communication, and the nose-to-brain pathway. Physiology and Behaviour, 83, 3-11.
  23. 23.0 23.1 McLaughlin. Nicole C.R. 2007. Odor identification deficits in frontal temporal dementia: A
  24. 24.0 24.1 24.2 Lamboin. S et all. 2007. Effects of anti-depressents on olfactory sensitivity in mice. Progress in Neuro-Psychopharmacology & Biological Psychiatry 32 (2008) 629–632.
  25. Atanasova. B, 2008. Olfaction: A potential cognitive marker of psychiatric disorder. Neuroscience and Biobehavioral Reviews 32 (2008) 1315–1325.
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