Download Chemosense in Mollusks

Olfaction
Invertebrate
- mollusks
- arthropods
Vertebrate
- main epithelium
- Vomerolfaction
Chemosense in Mollusks
• phylum Mollusca (70,000 species) includes
– Snails
– Clams
– Abalones
– Octopus
– Cuttlefish
– Nautilus
– Nudibranchs
• Terrestrial & aquatic
• Distance (= olfactory) & contact (= taste) chemosense
All of the “standard” olfaction functions found in mollusks.
– Locating food sources and tracking prey
– Mating
– Finding places for dens or hibernation
– Interspecies interaction
– Homing
Also important for settlement and metamorphosis in
marine gastropod larvae.
Terrestrial Gastropods
Stylommatophoran land snails
– Two pairs of olfactory tentacles + one pair of labial
palps for gustation.
– Use 2 pairs of tentacles to build a three-dimensional
odor landscape:
compare right to left and up to down along chemical
gradients. (Intensity is 3rd dimension)
Sophisticated!
Rosy Wolfsnail: carniverous – finds prey snails by tracking
their slime trails. White circles on olfactory chemosense
organs. In a population there are two olfactory phenotypes
that correlate with food preference.
Neural Paths in Snail Olfaction
• Snails dedicate a large number of neurons, relative to the
rest of their nervous system, to olfaction.
• Multiple serial and parallel pathways connecting the
olfactory organ with the integrative centers of the CNS.
• The tentacle ganglion contains a large number of
synapses.
• Olfactory axons from the tentacle ganglion terminate in
the procerebrum - a unique region of the snail for
olfactory processing.
Behavior experiments – what does the snail not like?
▪ Most of the snail’s reactions to the odors were negative
(avoidance response). The point is that a large number
of generic chemicals can be detected. Cross-react with
biologically relevant avoidance detector?
(Voss, M. 1999)
Single Neuron Response to Various Odors
One neuron has multiple specificities – similar
to vertebrate olfaction.
(Voss, M. 1999)
Aquatic gastropods – greater diversity of olfactory
receptor organs compared with terrestrial
gastropods.
Nudibranch Rhinophores
– note high surface area.
Example of specific chemosense in mollusk: Settlement /
Metamorphosis signal in Red Abalone (Haliotis rufescens)
Larvae
The larvae are induced to settle
in response to exogenous
GABA-like peptides found on the
surface of some algae.
Receptor dependent G-protein
transduction system to
determine when to settle from
the plankton and
metamorphose.
(Baxter, Gregroy T. et al, 1992)
A 7-TM receptor protein on
chemosensory neuron
dendrites binds lysine (&
GABA-like proteins).
(Baxter, Gregroy T. et al, 1992)
Cephalopods are the most advanced mollusks,
and have very well developed sensory
systems.
BUT…
They are more visually oriented, and olfaction
is actually reduced.
Cephalopods: Squid Olfactory Epithelium factoids
• Squid olfactory organ is small: 0.5 – 1.0
mm.diameter.
• Located ventrally and posteriorly to each eye
near the opening to the mantle cavity.
• Ciliated support cells sweep water towards the
receptor cells.
• Multiple cell types in olfactory organ: Mucusproducing goblet cells, basal cells and several
types of olfactory receptor neurons.
(Chen and Luchero, 1997)
Olfactory receptor neurons make connections with the
“optic gland”.
Olfactory groove
Sources
•
Rosy Wolfsnail picture:
–
•
Red Abalone picture:
–
•
•
•
•
•
•
http://www.travel-images.com/thai197_r.jpg
Amphid picture:
–
•
•
http://www.seaslugforum.net/factsheet.cfm?base=rhinonud
Fried egg nudibranch picture:
–
•
http://www.bigislandabalone.com/images/red-abalone-1.jpg
Rhinophore pictures:
–
•
http://www.columbia.edu/itc/cerc/danoff-burg/invasion_bio/inv_spp_summ/Euglandina_rosea.html
http://www.apsnet.org/education/IllustratedGlossary/PhotosA-D/amphid.htm
Atkinson, James W.
Baxter, Gregroy T. and Morse, Daniel E. “Cilia from Abalone Larvae Contain a Receptor Dependent G Protein Transduction System Similar to
that in Mammals”. Biology Bulletin 183: pg 147-154. August, 1992.
Chase, R. and Tolloczko, Z. “Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond.” Microscopy
Research and Technique. Feb. 15, 1993.
Chen, Nansheng. Lucero, Mary T. “Characterization of voltage and Ca2+ activated K+ channels in squid olfactory receptor neurons.” The Journal
of Experimental Biology 200: 1571-1586. 1997.
Chia, FS., Koss, R. “Fine structure of the larval rhinophores of the nudibranch, Rostanga pulchra, with emphasis on the sensory receptor cells.”
Cell Tissue Research225:235-248. 1982.
Eisten, Heather L. “Why are olfactory systems of different animals so similar?” Brain Behavior and evolution 59: 273-293. 2002.
http://www.msu.edu/~eisthen/lab/pubs/BBE2002b.pdf
Voss, M. “Neurophysiological and Behavioral Responses to Olfactory Stimuli in the Snail Helix pomatia L.” Physiological Response 49: 463-469.
2000. http://www.biomed.cas.cz/physiolres/pdf/2000/49_463.pdf
Arthropods
Insect Olfaction
Basics:
Odor molecules bind directly to a receptor protein or to
odor binding protein (OBP) which binds to the receptor
protein.
• OBP may improve diffusion to the dendrites.
• OBP may improve selectivity.
The receptor protein is part of a G-Protein membrane
signaling system.
What specifies the selectivity of the receptors and odor
binding proteins?
Only 100-200 7-TM different olfactory receptor
molecules.
Each neuron expresses only a small number of olfactory
receptor proteins.
Each neuron produces slightly different responsiveness.
The receptor combination makes the neurons sensitive /
selective to a wide variety of different chemicals and / or
combinations.
An odorant receptor (7-transmembrane G-protein-coupled
receptor)
(In humans domains 3-5 are
highly variable – about 350
isoforms of the gene.)
So domains 3-5 are probably
the odorant binding site.
The C-terminus and the intracellular loops I2 and I3 function
as G-protein binding domains.
http://www.cf.ac.uk/biosi/staff/jacob/teaching/sensory/olfact1.html
Drosophila olfactory bristles
1 micron
l,s = large,
small
basoconic
sensilla
A = antenna funniculus olfact. bristles
P = maxillary palp olfact. bristles
5 microns
Typical olfactory sensillum
Note multiporous
sensillum (gustatory are
uniporous).
http://www.kcl.ac.uk/ip/christerhogstrand/courses/hb0223/sensory.htm
Functional classification of odorant receptors in Drosophila
Use calcium indicator dye to observe active
neurons in the antennal lobe of the bee brain.
Olfactory neurons with functionally relevant
(together) sensitivities converge on the same
lobe neurons.
Unique pattern of activity for a particular odor or
composite.
Air puffs with different chemicals stimulated Honeybee
antennae while Ca2+ indicator dye was in brain neurons.
Mosquito CO2 & lactate detection
• Host-seeking in female
mosquitoes: detect CO2 and
lactic acid.
• CO2 and lactic acid
produced in highest
concentrations by
endotherms.
• CO2 more important for host
localization, lactate for host
preference.
http://www.sdbonline.org/fly/hjmuller/or83b-1.htm
• Odors detected by receptor neurons in
sensilla (cuticular extensions) situated on
the antenna and maxillary palps.
• Different types of antenna sensilla:
1. grooved peg sensilla (gp)
2. sensilla trichodea (St (I))
antennal sensillum
• Grooved peg sensilla are highly
responsive to odors present on human
skin or in human sweat, especially lactic
acid. Sensilla trichodea less so.
Anopheles gambiae
• CO2 sensitive sensilla have been located
primarily on the maxillary palps. Each
receptor contains 3 neurons.
maxillary palps
webdb.dmsc.moph.go.th/.../ pics/A_mosquito.jpg
CO2 Specific Receptors neurons in grooved-peg (basiconica)
sensilla
CO2 thresholds =150-300 ppm; ambient = 300-330 ppm 
sensors work down to baseline.
(background around 0.035%, vs 4% for exhaled CO2)
Steep concentration response functions: 50 ppm ∆  reliable
changes in neural activity.
Receptor response to step increases in CO2 concentration not
influenced by background CO2  absolute CO2 detectors
Sufficient dynamic range to cover CO2 concentration range
elicited by human hosts.
(Grant and O’Connell, 1996)
CO2 Behavioral Studies
• CO2 is a potent “activator” in mosquitos to begin hostseeking.
• Flight velocity  The higher the CO2 level, the faster the
mosquito flies.
• Upwind turning toward the potential host (Dekker, Geier,
and Carde; wind tunnel data)
• In A. aegypti, CO2 functions as a releaser for higher
sensitivity and responsiveness to skin odors.
Wind Tunnel Device Used For CO2 Behavioral Study
Fig. 1. Wind tunnel setup and plume generators. Superimposed ribbon plume generator (A), and the
continuous (see also Fig. 2) plume generators (B,C). The superimposed plume was generated by a pipette
positioned 100 cm downwind and 30 cm upwind of the release cage. This configuration created a ribbon
CO2 plume that passed through the centre of the release cage. The continuous plume generator (B) was
placed behind the stainless steel laminising screens. It had two inlets, one for the odour, and the other for a
4 l min–1 clean air `jet' to mix the mixture. We also tested a continuous skin odour plume by inserting a
hand from outside the wind tunnel directly in the continuous plume generator through a tube (C) upwind
from the laminising screens (Dekker et al., 2005).
Lactic Acid (LA) Specific Receptors
• Very little activity in response to other small, organic
acids.
• Human LA flux rate ≈ 1.5x10-12 moles/second, which is
well within the range of sensitivity of the LA receptor.
• Newly emerged females do not respond to LA, however,
as the females develop, there is a progressive increase
in LA receptor sensitivity. By the time females are of
host-seeking age (24 hours after emergence), the LA
receptors are sensitive to very low concentrations of LA.
(Stanley, 2005)
Attractiveness of different subjects: Not all skin rubbings
are equally attractive!
The order of
attractiveness is
subject A>B>C>D.
Figure 1 Comparison of odour samples obtained from four humans
(A–D) with respect to their attractiveness for yellow fever mosquitoes.
Values are means ± SE of 56 repeated bioassays with 20 (± 3)
mosquitoes, respectively. Significance levels: ***, P < 0.001; **, P <
0.01; ns, not significant.
Dose-Dependent Effects of Lactic Acid
▪Add 0.06 to 6.3 µg/min lactate to odor samples from subject C, testing
against subject A.
▪At 0.6 µg/min the attractiveness of the modified stimulus was doubled,
dose-dependent increase with larger lactate concentrations.
DEET blocks grooved-peg lactate sensors!
(N, N-diethyl-m-toluamide)
Mosquito refs.
Acree, F. Jr, Turner, R.B., Gouck, H.K., Beroza, M. and Smith, N. (1968) 1-Lactic acid: a mosquito attractant isolated from humans. Science, 161, 13461347.
Beaty, Lyric C. Host-Seeking Behavior in Hematophagous Mosquitoes (Diptera: Culicidae)
http://www.colostate.edu/Depts/Entomology/courses/en507/papers_1997/beaty.html
Bernier, U. R., Kline, D. L., Barnard, D. R., Schreck, C. E. and Yost, R. A. (2001). Analysis of human skin emanations by gas chromatography/mass
spectrometry. 2. Identification of volatile compounds that are candidate attractants for the yellow fever mosquito (Aedes aegypti). Anal. Chem.
72,747 -756.
Bowen, M. F. (1996). Sensory aspect of host location in mosquitoes. In CIBA Foundation Symp., 200, Olfaction in Mosquito-Host Interactions (ed. G. R.
Bock and G. Cardew), pp. 196-208. New York: John Wiley and Sons.
Dekker, T., Geier, M., Carde, R. (2005) Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odors. The Journal of
Experimental Biology 208, 2963-2972 (2005).
Geier, M. and Boeckh, J. (1999) A new Y-tube olfactometer for mosquitoes to measure the attractiveness of host odours. Entomol. Exp. Appl., 92, 9-19.
Geier, M., Sass, H., and Boeckh, J. (1996) A search for components in human body odour that attracts females of Aedes
aegypti. In Cardew,
G. and Goode, J. (eds), Mosquito Olfaction and Olfactory-Mediated Mosquito-Host Interactions, Ciba Foundation Symposium 200. John Wiley &
Sons, New York, pp. 132-144.
Grant, AJ. And O’Connell, RJ. (1996) Electrophysiological responses from receptor neurons in mosquito maxillary palp sensilla. Ciba Found Symp.
1996; 200: 233-48; discussion 248-53, 281-4.
Hohorst, H.J. (1970) L-(-)-Laktat. Bestimmung mit Laktat-Dehydrogenase und NAD. In Bergmyer, H. (ed.), Methoden der enzymatischen Analyse, 2nd
Edn. Verlag Chemie, Weinheim, Germany, Vol. 1, pp. 1425-1437
Mackie, Ryan. Long-Range Orientation, Selection of Biting Sites, and Chemical and Visual Cues Associated with Host-Seeking Behavior in Mosquitoes
(Diptera: Culicidae). http://www.colostate.edu/Depts/Entomology/courses/en507/papers_1999/mackie.htm
Meijerink, J. and Van Loon, J. J. A. (1999). Sensitivities of antennal olfactory neurons of the malaria mosquito, Anopheles gambiae, to carboxylic acids.
J. Insect Physiol. 45,365 -373.
Pappenberger, B., Geier, M. and Boeckh, J. (1996). Responses of antennal olfactory receptors to odours from the human body in the yellow fever
mosquito, Aedes aegypti. In Ciba Foundation Symposium vol.200 (ed. G. R. Bock and G. Cardew), pp.254
Qiu, Yu Tong. Sensory and behavioral responses of the malaria mosquito Anopheles gambiae to human odours; dissertation no. 3858. Wageningen
University. December 2, 2005. 13 March 2006<http://library.wur.nl/wda/abstracts/ab3858.html>
Stange, G. (1999) Carbon-dioxide sensing structures in terrestrial arthropods. Microscopy Research and Technique. Volume 47, Issue 6, pg 416-427.
Stange, G. (1996) Sensory and behavioural responses of terrestrial invertebrates to biogenic carbon dioxide gradients. In Stanhill, G. (ed.), Advances in
Bioclimatology. Springer, Heidelberg, Vol. 4, pp. 223–253.
Stanley, D. (2005) Lecture 28: Chemical Communication-Insect Olfaction. 13 March 2006 <http://lhs.lps.org/staff/sputnam/Ent801/Lec_notes.htm>
Steib, B., Geier, M., and Boeckh, J. (2001) The Effect of Lactic Acid on Odour-Related Host Preference of Yellow Fever Mosquitoes. Chem. Senses.,
26, 523-528.
Zweibel, L.J. The Biochemistry of Odor Detection and its Future Prospects. Vanderbilt University. 10 Mar 2006
<http://www.biol.sc.edu/~vogt/PB/zwiebel-PB.pdf#search='Gprotein%20coupledreceptor%2C%20mosquitoes‘>
Vertebrate olfaction
fish
Some better fish noses
Isosmate fish (slow
swimmers – catfish,
dogfish and the eel,
left) use ciliated cells
to move water across
the epithelium – up to
15 mm/s water
velocity.
Cyclosmate fish pump water with muscular contraction.
A large portion of the fish
brain devoted to smell in
lampreys.
Olfactory Imprinting in Salmonids
Imprint on odors: 2-week period before returning to
ocean (ca 2 yrs old; Parr-to-Smolt transition).
Can train captured smolts to discriminate between
water from different streams. Discrimination
disappears if cauterize nose.
Transplant fish from stream A to stream B during
imprinting period. Transplants return to stream B as
adults to spawn.
Reference: Hasler, Schotz, Horrall: Olfactory Imprinting and Homing in Salmon. American Scientist 66:347-355
Olfactory Imprinting in Salmonids
Experimental group (16000!!!) of marked (fin-clipped)
smolts exposed to artificial compound (morpholine,
C4H9NO).
Eighteen months later, an artificial stream constructed
and small amounts of morpholine released into it.
Of adult fish entering artificial stream, 89% were from
the experimental group.
So – no genetic preference for one stream or another.
Reference: Hasler, Schotz, Horrall: Olfactory Imprinting and Homing in Salmon. American Scientist 66:347-355
Electrophysiological thresholds for some odorants
in salmonids.
Species
Oncorhynchus mykiss
(Rainbow Trout)
Threshold (M)
Amino Acids
Steroids
10-8 - 10-7
10-10 - 10-9
10-16 (a)
Salmo gairdneri
(Steelhead)
Oncorhynchus nerka
(sockeye)
10-7 - 10-6
Oncorhynchus kisutch
(coho)
10-7 - 10-6
(a) Gonadotropin-releasing hormone (GnRH)
Amphibians
- Urodeles are specialists, anurans typically
poor.
Large main olfactory chamber in a
salamander (Dicamptodon tenebrosus).
larval
adult
Salamander refs.
http://www.people.eku.edu/ritchisong/birdbrain.html
http://academic.scranton.edu/faculty/GOMEZG2/avianorn.htm
http://instruct1.cit.cornell.edu/courses/psych396/student2002/hcs7/
http://instruct1.cit.cornell.edu/courses/bionb424/students/jlk35/
http://digimorph.org/specimens/Nephrurus_levis/
http://elibrary.unm.edu/sora/Auk/v085n01/p0055-p0061.pdf
http://www.mercurybay.co.nz/local/kiwiinfo.html
http://www.ento.csiro.au/education/insects/dermaptera.html
Stuelpnagel, Jeremy T., Reiss, John O. (2005) Olfactory Metamorphosis in the Coastal GiantSalamander (Dicamptodon tenebrosus),
Journal of Morphology, Volume 266 (p 22-45)
Reid, Brian, Ordish, G., and Harrison, M. (1982) An analysis of the Gizzard Content of 50 North Island Brown Kiwis, Apteryx Australis
mantelli, and notes on Feeding Observation, The New Zealand Journal of Ecology, Volume 5 (p 76-85)
Duchamp-Viret, Patricia, Duchamp, André, and Chaput, Michel A. (March 15, 2000) Peripheral Odor Coding in the Rat and Frog: Quality
and Intensity Specification, The Journal of Neuroscience Volume 20 issue 6 (p 2383-2390)
Dial, Benjamin E., Schwenk, Kurt (1996) Olfaction and Predator Detection in CoZeonyx breuis (Squamata: Eublepharidae), The Journal of
Experimental Zoology, Volume 276 issue 6(p 415-424)
Reptiles
Snakes: Both main &
vomerolfactory epithelia.
Main: odors come in
through nostrils: Long
range, general olfactory
sense.
In the lizard world, Gekkos are the olfactory
specialists.
Why?
Geckos use nasal olfaction to detect predator species
(snakes).
Increased behavioral response to chemical stimuli from a
predator snake species (H. torquata).
birds
In general, birds are boring from an olfactory
perspective, but these bird species do have
more specialized abilities:
1. Kiwis
2. Petrels
3. Small new-world vultures: e.g. turkey
vultures
As birds evolve from reptiles: OB smaller % of brain,
Optic Lobe larger % of brain.
Our bird specialists:
Food (carrion) finding -Vultures: detect the smell of carrion based on
emission of the gas ethyl mercaptan
Albatrosses and petrels: detect dimethyl sulfide.
Food (worms) finding –
Kiwi (poor vision, nocturnal) – smells worms
Orientation and navigation
Leach's Petrel: nest odor used to find nest while
flying at night. They can find offspring if the
offspring are moved.
Kiwi
Nostril at end of bill
Detects a few ppm of odorants given off by
underground insect or worm.
Kiwi – largest bird olfactory bulb
Kiwi OB 2X next
closest species
Runner-up birds: olfactory bulb size shown in brains that are
all scaled to same size.
Petrel is next best – detect odors of dead stuff floating on the
ocean.
Petrel turbinate bones – larger
& more elaborate than other
birds.
(http://academic.scranton.edu/faculty/GOMEZG2/avianorn.htm)
Mammals: Olfactory specialists of
the vertebrates.
TAXON
NUMBER OF
OLFACTORY
PROTEIN
VARIANTS1
OLFACTORY
AREA OF
EPITHELIUM SIZE & DENDRITE
No. RECEPTORS
CILIA (cm2)
Fish2
Humans
100
1-2 cm2
12 million
20
Mice
Dogs
Elephants
350
1000
5-10 m2
4 billion
100,000
(100 sq ft of
dendrite
membrane)
100 m2
& 5 x 105
receptors/mm2
1,000,000 m2
(1076 sq feet of
dendrite
membrane!)
1
2
based on the number of genes coding for variants
very small sample size, not including olfactory specialists
Resolving power of mammalian olfactory system is
impressive, even in humans:
Left and right stereoisomers of carvone are
perceived as spearmint and caraway,
respectively
Sensitivity in humans not too bad either –
about 10-11 M for some chemcials.
Vertebrate olfactory receptor neurons.
Express genes that code for receptor
proteins, installed in dendrite
membrane.
All olfactory genes in vertebrates are homologs.
Olfactory receptor genes first appear in
amphioxus (cephalochordate).
So…
Olfactory system evolved to detect stuff in water!
Main classes of odorant molecules in water:
- amino acids (food)
- bile acids (social communication)
- Nucleotides
- Steroids (reproductive behavior)
- Prostaglandins
(all non-volatile, charged molecules)
Main classes of odorant molecules in air:
- Volatile, non-charged chemicals.
Teleosts – Relatively small number of OR genes.
Coelacanth – 300 genes (>> teleosts; = birds)
Pre-adaptation for tetrapods??!!
No one is clear about the evolutionary jump
from aquatic to terrestrial odor detection in
vertebrates!
Binding to transmembrane
proteins: GPCR  incr.
cAMP
cAMP controlled Na+,
Ca2+ conductance.
Also cAMP dependent Clchannel.
Basic Neurochemistry: Molecular, Cellular and Medical Aspects. 6th edition.Siegel GJ, Agranoff BW, Albers RW, et al.,
editors. Philadelphia: Lippincott-Raven; 1999.
Ions flowing through
transduction channels come
from the mucous layer.
Prolonged swimming  wash
out mucous  temporary
anosmia.
Ca2+ entry activates β-arrestin
 adaptation.
Basic Neurochemistry: Molecular, Cellular and Medical Aspects. 6th edition.Siegel GJ, Agranoff BW, Albers RW, et al.,
editors. Philadelphia: Lippincott-Raven; 1999.
CNG-coupled receptor transduction:
Na+ Ca2+
Where are the olfactory neurons in
vertebrates?
Human olfactory epithelium and bulb
Olfactory receptor cells are NOT secondary receptors,
rather they are neurons.
Overall plan of mammalian olfaction
Organization of neurons in one glomerulus
efferent control
Olfactory Tract
Granule Cell Layer
Mitral Cell Layer
External Plexiform Layer
Glomerular Layer
Olfactory Nerve Axons
M = mitral cell, T = tufted cell, PG = periglomerular cell, Gd, Gs = deep &
superficial granule cells, respectively
Descending input disinhibits mitral cells in hungry
rats.
Olfactory bulb looks like
a retina in terms of cell
types and connections.
Implies a contrast
enhancement
mechanism through
lateral inhibition.
Evidence for oscillations in OB (rapid descending input).
Associated with “fill-in-the-gap” learning mechanism.
Rats have 1800 glomeruli in their olfactory bulb.
One rat glomerulus: 125 mitral cells, 150 tufted cells (Overall 300 – 400
neurons)
Convergence of 25,000 axon branches from olfactory neurons to 1800
glomeruli.
Somehow each olfactory neuron “knows” its chemical preference.
Those with similar preference synapse on the same glomerulus.
How many smells?
A very large gene family codes for olfactory
receptor proteins:
100 in fish
500 – 700 in humans
1000 in rats and mice, = 5% of the entire
genome!
Hypothetical arrangement:
Neuron 1 expresses receptor 1 -- binds to five
different odors that share a similar chemical structure:
A, B, C, D, E
Neuron 2 expresses receptor 2 -- binds 2 different
odors: F, G
Neuron 3 expresses receptor 3 -- binds B, H, I.
Note neuron 1 and 3 share sensitivity to B. Each
would send an axon branch to a common glomerulus,
which would be an odor B (and a few others)
specialist.
A simplistic model of
how olfactory patterns
could be generated.
Still, 1000 genes can’t account for the number
of odors detectable.
Theory, until recently, was that posttranscriptional re-arrangement (same
mechanism that creates hypervariable regions
of antibodies) led to a wider variation of binding
possibilities.
Recent data show no such re-arrangement, but
there is not an alternative hypothesis!!
Olfactory receptor neurons that express a
particular gene are labeled.
Tremendous convergence onto glomeruli.
Olfactory neurons
engineered to have a
particular gene (M72) and
to produce green
fluorescent protein.
The M72 neurons send
axons to 4 glomeruli in
different parts of the bulb.
From Gordon Fain
Photomicrograph of Rat olfactory bulb (left) –
control (no smell)
Same shot, but smelling peanut butter (right) –
subtractive image
Activity of neurons in rat OB when stimulated with
acids and alcohols.
Systematic change in chain length – glomerulus
pattern shifts for each chemical
Specialized chemoreception
– pheromones and vomerolfaction.
Specialized chemodetection
Allomone: Organism 1 makes a chemical signal to its benefit,
but not to the benefit of the receiver. Example: Aposematic
signal  I am distasteful.
Kairomone: Organism 1 makes a specific signal that is
intercepted by, say, a predator. Benefit to receiver, not to
sender.
Synomone: Both sender and receiver profit from specific
chemical. A plant that releases a signal for a pollinator.
Apneumone: Chemicals released by dead stuff that attracts a
carrion feeder.
Pheromone detection
note astonishing
sensitivity
Large surface area!
Enormous amount of convergence
Extreme signal/noise ratio
Sensitivity at limit of physical phenomenon
Vomeronasal system – in most (?)
vertebrates.
Particularly well developed in snakes and
mammals.
VNO projects to the Accessory Olfactory Bulb
(AOB), and then projections to various brain
regions.
Blue: Pathways
activated in rodents by
cat kairomones
Red: Conspecific
mouse odors
BST: Bed nucleus of the stria terminalis
AA: Anterior amygdala
BAOT: Bed nucleus of the accessory olfactory tract
MEA: Medial amygdala
VMH:
VNO – 4 neuron subtypes.
Phospholipase-C mediated
signaling, TRPC2 channel
(Main Olfactory Epithelium – 6
subtypes. cAMP signaling, CNG
channel.)
VNO neuron receptor proteins –
much more species-specific
divergence  taxon specific
chemosense. MOE = general
purpose, everyone has roughly
the same.
FPR:
formyl peptide
receptor
From: Chemosensory Transduction: The Detection of Odors, Tastes, and
Other Chemostimuli. Edited by Frank Zufall, Steven D. Munger. Elsevier, 2016
Kinds of ligands that bind to VNO neurons:
1. Exocrine gland peptides (e.g., stuff in tears)
2. Formyl peptides (health status detection?)
3. MHC class 1 peptides (secreted in urine)
4. Major urinary proteins (MUP)
5. Volatile small molecules
6. Sulfated steroids
Rodents express many 100’s of V1Rs, V2Rs &
formyl FPRs.
Each may be specialized for a particular
chemical detected and function.
Example: “Darcin” - a MUP
- only in male mice.
- Secretion depends on concentration of
testosterone and growth hormone.
Specifically, detection of Darcin by male mice
leads to high aggression.
Note that MHC proteins provide individual
recognition.
Not surprising that a lot of VNO associated
with social behavior.
Next 2 slides: Summary of current known VNO
chemical detection…
Specialized detection not the exclusive province of
the VNO
Kairomones – inter-species specific chemical
communication.
Detectopm can be mediated by the MOE.
So… VNO for specialized chemical detection
BUT specialized chemicals can also be
detected by MOE.
How does the
MOE do it?
Some MOE neurons don’t express “standard”
receptors.
Instead express: Trace amine associated
receptors (TAARs).
Respond to volatile amines found in urine of
predators.
Example: trimethylamine
Final complication:
2-heptanone (MUP from male urine, assoc.
with social behavior) detected by both MOE &
VNO.
In snakes “double”
pyramidal cells in
lateral cortex (LC)
have dendritic
arbors extending
to both the main
olfactory region
and the
vomerolfactory
region.
Reminiscent of the
I.R. and vision
integration in pit
vipers!
Fish through mammals produce
pheromones, detected by the MOE, or
AOE, or both depending on the
species.
Fish, though, also have specialized
chemodetector cells other places…
Fish secrete alarm pheromones
Club cells (alarm substance cell, ASC) in the skin
detect the pheromone hypoxanthine-3(N)-oxide
(a purine).
Leads to aversive behavior in fish detecting it.
ASC
Minnow
skin x.s.
Chivers et al. Proc. R. Soc. B
(2007) 274, 2611–2619