Sensory Encoding of Smell in the Olfactory System of MAMMALS
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1 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
2 TODAY Compare / contrast! Gross Pathways Receptor Neurons Glomeruli Output Neurons Higher centers
3 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)
4 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?
5 Quiz!
6 Olfactory Organs Mammals: 4 organs Main Olfactory Epithelium Vomeronasal Organ Grueneberg ganglion Septal organ of Masera Insects: 2 organs Antennae Maxillary Palps
7 Mammalian Olfactory Organs and Receptors
8 Main Olfactory Epithelium MOE X X X ORs for odor ID; functional genes Trace amine-associated receptors (TAARs) can detect volatile urine-based amines; 15 in mouse (social cues) Output to main olfactory bulb
9 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
10 Gruenberg Ganglion X Trace amine-associated receptors (TAARs) ONE V2R receptor Responsive to mechanical stimulation (sniffing / air puffs) Outputs to main olfactory bulb
11 Septal Organ of Masera X ORs for general alerting Responsive to mechanical stimulation (sniffing / air puffs) Outputs to main olfactory bulb
12 Insect Olfactory Organs and Receptors
13 Antennae Basiconic for odor recognition, repulsion behavior Ors A few Grs (CO2) Coleoconic (function unknown) Keene & Waddel (2007) Ionotropic receptors derived from glutamate receptors! Trichoid for pheromones
14 Maxillary Palps Keene & Waddel (2007) Basiconic sensillia for taste enhancement
15 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)
16 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
17 ORN Activity vs Concentration Kreher et al (2008)
18 ORN Activity vs Concentration Kreher et al (2008)
19 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
20 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!
21 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)
22 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
23 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)
24 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)
25 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
26 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
27 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)
28 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)
29 Review: Transformations Two glomerular transformations: Increasing signal-to-noise Producing variable gain PN / Kenyon Cell Transformations: Decorrelation of ORN signals
30 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
31 Decorrelation
32 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)
33 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 ( coincident Pns) Loss of oscillations in bees no fine discriminations Fig. 7 from Masse et al (2009)
34
35 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)
36 Higher-level pathways
37 Olfactory Learning Li et al (2008)
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