Transcript www.cogsci.ucsd.edu

Sensory Encoding of Smell
in the Olfactory System of MAMMALS
(reviewing “Olfactory Perception: Receptors, Cells, and Circuits” by
Su et al, 2009)
Ben Cipollini
COGS 160
May 13, 2010
TODAY

Compare / contrast!

Gross Pathways

Receptor Neurons

Glomeruli

Output Neurons

Higher centers
Gross Pathways





ORNs in antennae
Projection neurons from
antenna lobe to lateral horn
and mushroom body
Glomeruli in antenna lobe
mediate most receptorspecific processing
Kenyon cells in mushroom
body have sparse
representation of odors for
associative learning
Lateral horn has placespecific processing of
sensory-motor associations
Keene & Waddel (2007)
Compare to Mammals
Shared Feature
Insect
Mammal
ORNs
Antenna +
maxillary palps
Olfactory
epithelium
Glomeruli
Antenna lobe
Olfactory bulb
Output cells
Projection
Neurons
Mitral cells &
Tufted cells
Classification &
learning
Mushroom body
Piriform Cortex
DM Thalamus
Behavioral outputs
Lateral Horn
Orbitofrontal ctx?
Quiz!
Olfactory Organs

Mammals: 4 organs

Main Olfactory
Epithelium

Vomeronasal Organ

Grueneberg ganglion

Septal organ of
Masera

Insects: 2 organs

Antennae

Maxillary Palps
Mammalian Olfactory
Organs and Receptors
Main Olfactory Epithelium

MOE


X
X

X
ORs for odor ID; 250-1200
functional genes
Trace amine-associated
receptors (TAARs) can
detect volatile urine-based
amines; 15 in mouse (social
cues)
Output to main olfactory bulb
Vomeronasal Organ




V1Rs (urine) for
conspecific recognition,
male sexual behavior,
maternal aggression,
regulation of female
estrous cycles, stress
level indicator
V2Rs (sweat and urine)
for pregnancy blocking,
individual / gender
identity, aggression
(from males), stress
(from females)
Formyl Peptide
Receptors (immune
system) for health status
Outputs to accessory
olfactory bulb
Gruenberg Ganglion


X


Trace amine-associated
receptors (TAARs)
ONE V2R receptor
Responsive to mechanical
stimulation (sniffing / air
puffs)
Outputs to main olfactory
bulb
Septal Organ of Masera


X

ORs for general alerting
Responsive to mechanical
stimulation (sniffing / air
puffs)
Outputs to main olfactory
bulb
Insect Olfactory
Organs and Receptors
Antennae


Basiconic for odor recognition,
repulsion behavior

60-340 Ors

A few Grs (CO2)
Coleoconic (function unknown)


Keene & Waddel (2007)
Ionotropic receptors →
derived from glutamate
receptors!
Trichoid for pheromones
Maxillary Palps

Keene & Waddel (2007)
Basiconic sensillia for
taste enhancement
The Evolutionary Story

Insects




Finding homologies in species of the same
order can be challenging
Probably fast evolution
Mechanism (duplication & variation vs.
modification) unknown
NOTE: loss of a single OR doesn't necessarily
eliminate associated behavior


Ensemble encoding
Different ORs coding for an odor at different
concentrations (helps with variable gain)
Review: Tuning Curves of ORNs

Odorants are identified by the
pattern of receptors activated


Individual receptors are activated
by subsets of odorants




Hallem et al (2006)
Including inhibition of tonic firing
Receptors lie along a smooth
continuum of tuning breadths
Broadly tuned receptors are most
sensitive to structurally similar
odorants
Higher concentrations of odorants
elicit activity from greater numbers of
receptors
Odor intensity as well as odor
identity is represented by the
number of activated receptors
ORN Activity vs Concentration
Kreher et al (2008)
ORN Activity vs Concentration
Kreher et al (2008)
Evolution II: Pseudogenization

Humans

20-30% of ORs

90% of VRN1s

100% (so far) of
VRN2s (only 20
genes exist)

Aquatic vertebrates


Terrestrial vertebrates


Only have OR class I
Have OR class I & II
Dolphins


Have class I
100% of OR class II
pseudogenized
For no particular reason...

3 cool properties of ORNs that were discussed
in this paper:

Temporal tuning curves

Antagonistic ORNs!

Insect ORNs are actually really weird!
Tuning Curves of ORNs (New):
Temporal Dynamics


Different ORNs can have
different temporal dynamics
(even for the same odor)
A single ORN can have different
temporal dynamics to different
odors
Odorant tuning curves
Bruyne et al (2001)
Combinatorics: Antagonistic Inhibition

The perceived magnitude of an
odorant mixture was neither
additive nor a simple average of its
components




Masking (i.e. modification of perceived
odor) or counteraction (i.e. reduction
of odor intensity).
Mixing some odorants led to the
emergence of novel perceptual
qualities that were not present in
each individual odorant

Oka et al (2004)
Fell between these limits, due to:
Suggests that odorant mixture
interactions occurred at some levels in
the olfactory system
Observed at presynaptic ORN
axons in olfactory bulb
Insects ORNs are CRAAAZY!



Insect odor receptors have 7 transmembrane domains
and have long been assumed to be GPCRs.
BUT we see major major differences!

No G protein mutant has been found to suffer a severe loss
of olfactory function.

The topology of the insect Ors is inverted relative to GPCRs.

Each OR also appears to form a heteromultimer with Or83b
A canonical OR (with Or83b), can form a “ligand-gated
cation channel”


Due to an odorant-induced, rapidly developing, transient
inward current, independent of G protein signaling
A second, slower and larger component to the odorantinduced inward current

Slower both in onset and decay kinetics

Is sensitive to inhibition by a GDP analog
Siegel et al (1999)
ORN Transduction: “canonical”






Odorant binds to the odor
receptor
Odor receptor changes shape and
binds/activates an “olfactory-type”
G protein
G protein activates the lyase adenylate cyclase (LAC)
LAC converts ATP into cAMP
cAMP opens cyclic nucleotidegated ion channels
Calcium and sodium ions to enter
into the cell, depolarizing the ORN
• Calcium-dependent chlorine
channels contribute to
depolarization as well

G protein turned off by GDP
Firestein & Menini (1999)
Review: Projection Neurons




Live in antenna lobe (~200 per)
Receive input from ALL ORNs of a
single class (~50; ~25 from each
side)
Despite convergent input, show
broader odorant tuning than ORNs
Project out to “higher centers”:
mushroom body & lateral horn
Tufted & Mitral Cells





Live in olfactory bulb
Receive input from ALL
ORNs of a single class
from a single side
Like insect projection
neurons, show broader
odorant tuning than ORNs
Like insect projection
neurons, project out to
“higher centers”
NOTE: only mitral cells
project to posterior piriform
cortex
Review: Glomeruli


In Antenna Lobe, one per
odorant “class” (50)
Consist of:

Axons of ORNs

Dendrites of projection neurons


Mammalian Glomeruli
Neurites (axons and dendrites) of
local neurons
ORN inputs all from same
“class”, come bilaterally
Kandel, Jessel, Schwartz (2000)
Glomeruli:
MAMMALIAN
INSECT

50:1 convergence

5000:1 convergence

Pns input from 1

M/T input from 1


Interglomerular inhibition (local
neurons)
Intraglomerular inhibition (local
neurons)


Interglomerular inhibition (granule
cells)
Intraglomerular inhibition
(juxtaglomerular cells)
Review: Transformations


Two glomerular
transformations:

Increasing signal-to-noise

Producing variable gain
PN / Kenyon Cell
Transformations:

Decorrelation of ORN
signals
Variable Gain Revisited

Broader tuning widths and nonlinear amplification among projection neurons
are mainly due to strong ORN-projection neuron synapses
How?


Low Activity Amplification: Weak presynaptic ORN activity is sufficient to
trigger robust neurotransmitter release and cause substantial PN
responses.
High Activity Fall-off: Strong ORN activity leads to depletion of synaptic
neurotransmitter.
How about mammals?


The strong synapses : due to presence of numerous synaptic vesicle
release sites and a high release probability
High probabilities of vesicle release have also been found in the
mammalian olfactory bulb
Sparse Coding in Kenyon Cells

IN THE LOCUST


PNs (columns)
respond to most
odorants; KCs
(columns) respond to
very few
“Population
sparseness” - % of
cells that do NOT
respond to an odor
(rows)
Perez-Orive et al (2002)
How Do Locust KCs Become Sparse?






High convergence (400:1,
50% of PNs!)
Weak unitary synaptic
connections
Synaptic integration in
(oscillatory) time windows
Voltage-gated channels
amplify coincident spikes
High spiking threshold
(50-100 coincident Pns)
Loss of oscillations in
bees → no “fine”
discriminations
Fig. 7 from Masse et al (2009)
Higher-level pathways



Posterior Piriform cortex does
classification (like Mushroom
body!)
Cells within PPC project to
MOST areas that are
connected to
This includes feedback
projections to olfactory bulb
Johnson et al (2000)
Higher-level pathways
Olfactory Learning
Li et al (2008)