Journal club: olfactory perception, communication, and the nose-to-brain pathway
Consultation-Liaison Rounds, 05-3-3, at the SMBD – Jewish General Hospital
Article: Stockhorst, U., and R. Pietrowsky (2004) Physiol Behav 83:3-11.
Olfactory perception, communication, and the nose-to-brain pathway.
Abstract: The present paper’s aim is of to give an overview about the basic knowledge as well as actual topics of olfaction–with a special regard on behavior. We summarize different functions of the nose and the olfactory system in human physiology and psychology. We will first describe the functional anatomy of the olfactory system in man. Afterwards, the function of the olfactory system will be viewed from an evolutionary and phylogenetic perspective. We will further outline the main features of olfactory perception, and will show how olfactory perception is influenced by learning. Olfactory signals are relevant stimuli that affect communication. Consequently, the role of the olfactory system in social interaction and mood will be described and gender differences will be addressed. Finally, the function of the nose as an interface to the brain, including implications for pharmacology, will be discussed.
Discussion:
four systems involved in olfaction:
1. main olfactory system – for smelling volatile chemicals
2. trigeminal system – for perception of cold, pungent or burning sensations
3. accessory olfactory system – perception of non-smelling and non-volatile substances
4. terminal nerve – possibly related to reproductive behaviour. Chemosensory input stimulates release of LHRH.
Olfaction: phylogenetically very old, essential for within-species communication, food detection, recognition of enemies, recognition of toxins.
Functions well without any participation of conscious thought.
Although we assume that visual and auditory communication has supplanted olfactory communication in humans, this belief may simply be an artifact of the fact that visual and auditory communication take place within consciousness.
Example: being attracted to someone of the opposite sex at a party. People engage in flirting behaviours quite unconsciously. If the attraction results in a relationship, we might say “love at first sight” but it could have been “love at first smell”. It is only very recently that research is being done on seeing whether there are physiologic responses to chemicals at which are considered odourless. It should be noted that odour has meaning only in terms of a conscious response. If we are not consciously aware of a volatile chemical in our environment, there are at least 4 possible explanations:
1. it may mean that we do not have receptors for that molecule
2. it could be that the concentration is below threshold for conscious awareness
3. it could be that we have not yet “learned” to become consciously aware of the substance (eg, urine smell after eating asparagus)
4. it could also be that the there is no connection between the sensory and behaviour circuits and centers of conscious thought in the brain; this seems true of many reproduction-related behaviours, eg erectile tissue responses
the last explanation is the one most likely to cause us to think that the communication medium is no longer important in humans.
The article mentions 4 olfactory systems, but in fact talks about a fifth system: receptors for steroidal and peptide hormones in parts of the brain close to the nasal cavity, with the demonstrated capacity of these hormones to diffuse or to be transported from the nasal cavity directly into the brain through the cribriform plate, and get distributed to the brain receptors possibly by the CSF. This would be difficult to block experimentally, and would explain why reproductive behaviour manages to happen even when the olfactory systems are disabled. If we don’t take this system into account, we are likely to say that the olfactory systems are not that important in primates.
smell sensitivity: a moth can sense as little as 6 molecules of certain substances, eg pheromones
humans can perceive mercaptan at a concentration of 7×10 to the -13 Molar. (7x10E-13 x 6.02x10E23=4.2x10E11 M,
experiment: insulin injected into healthy male volunteers, at the same time as presentation of a smell, for 4 days. On 5th day, smell only; result: blood sugar fell (Classical conditioning). What about for pain control?
Females can discriminate between high symmetry males and low symmetry males when ovulating, but not when infertile.
Fluctuating asymmetry (small, random departures from bilateral symmetry) have been found to vary predictably with environmental quality, stress during development, inbreeding, heterozygosity.
What do I find interesting about the article:
1. the nose as interface to the brain. What is the possible functional significance of this capacity to respond to intranasal peptide hormones, such as insulin or oxytocin, which do not occur naturally in the environment? One possible answer is that these substances are secreted in urine (eg oxytocin, vasopressin). The fetus (and presumably the infant) secrete oxytocin in urine – this may prompt the tend-and-befriend response in its mother and of course the milk let-down reflex.
Vasopressin is involved in pair-bonding, eg in prairie voles which mate for life after a single night of cohabitation. This seems to be mediated by vasopressin and reward circuitry (oxytocin brain receptors are also implicated). Vasopressin is also secreted in urine, in fact urinary vasopressin is the usual lab test for this hormone. The vasopressin distribution in the brain of the prairie vole is also implicated in paternal care behaviour.
the meadow vole, however, has a different distribution of vasopressin and oxytocin receptors in its brain, and it has multiple sex partners. Thus, the behavioural effects of any of these neuroactive peptide hormones could be very species-specific.
Cholecystokinin is the most abundant neuropeptide in the CNS. It induces satiety in lab animals. Other effects are unknown. Aberrations of CCK expression or receptors may play a role in anxiety, panic, depression, analgesia, exploratory behaviour, vigilance, defensive rage, and memorisation, and interacts with dopamine, serotonin, endorphin, and GABA systems.
Temporal effects may be important, for example, which stimulus is detected first, and by which system. Example: in a given part of the brain, learning takes place best if certain events occur in sequence. In childbirth, there will be eg in the mother circulating fetal oxytocin from the fetal blood, via the placenta, prior to birth. The amniotic fluid also contains fetal oxytocin from fetal body fluids, as well as cell surface proteins with MHC information (major histocompatibility complex). This information is available to the mother after membrane rupture. Vaginal delivery stimulates endorphin systems (exercise, breathing, pain). Once the baby is born, in some species the mother eats the placenta and will also lick the baby clean. Finally, the baby’s urine contains oxytocin which may stimulate maternal lactation, shrinkage of the uterus, and tend-and-befriend behaviours.
In mice, major urinary proteins (MUP) are used to identify individuals, via the nonvolatile vomeronasal system, not MHC contrary to what was thought Cheetham SA, Thom MD, Jury F, Ollier WE, Beynon RJ, Hurst JL. The genetic basis of individual-recognition signals in the mouse. Curr Biol. 2007;17:1771-1777.
One can imagine that the effect of oxytocin might be different depending on how it’s delivered to the brain (via the maternal circulation or via the direct path from the nasal cavity to the brain); whether it arrives at the same time, before, or after the endorphin signal, whether it occurs together with other substances produced by the baby at the time of delivery or after delivery. Thus, oxytocin could play roles in facilitating uterine contraction during delivery, lactation after delivery, and learning of the specific pair bond between mother and offspring. This makes experimental manipulation extraordinarily complex.
The article also points out how some of the reproductive effects of pheromone substances are abolished by the use of oral contraceptives. But there may be other factors:
– use of antibacterial soaps may change the skin flora affecting the conversion of steroids into pheromonal substances.
– deodorants and antiperspirants may interfere with chemical signalling;
– it is likely that axillary hair, as well as head hair and pubic hair, plays a role in the diffusion of olfactory substances by greatly increasing the surface area available for evaporation. Shaving of axillary hair might reduce the effectiveness of the reproductive communication systems.
All of these factors could play a role in weakening possible effects in naturalistic experimental settings, eg the women’s dorm in which menstrual cycles tend to synchronize.