Lulu Bi / CNS 150 Lecture 16 Wednesday, November 5, 2014 Olfaction Bruce Cohen Reading: Kandel Chapter 32, pp 625-636 (not taste) 1 Olfactory memory •The nose can detect and (in principle) classify thousands of different compounds. •The ‘mapping’ of these compounds probably occurs by matching to memory templates stored in the brain • A smell is categorized based on one’s previous experiences of it and on the other sensory stimuli correlated with its appearance. 2 Olfactory system can distinguish stereoisomers of a compound Carvone Stereo center •The nose can distinguish similar compounds, such as chemical isomers, as different smells. •An example: the two stereoisomers of carvone smell like spearmint (R) and caraway (S). •This implies that there are stereoisomer-specific carvone receptors. •Also implies that odorant receptors are proteins 3 Anatomy of the mammalian olfactory system In many mammals (rodent shown here), the olfactory organs within the nose are split into the main olfactory epithelium (MOE) and the vomeronasal organ (VNO). MOE neurons project to the main olfactory bulb (MOB). VNO neurons project to the accessory olfactory bulb (AOB). MOB output neurons project to regions of cortex, while AOB output neurons project only to the (ventral) amygdala. 4 Cells of the mammalian main olfactory epithelium To olfactory bulb Basal cells Axon Olfactory neurons have apical dendrites with long ciliary extensions, where the transduction components are located. Olfactory sensory neuron Dendrite Supporting cells Mucus Cilia are embedded in the mucus layer. Olfactory neurons turn over and are replaced every 60 days. Cilia Figure 32-2 5 Olfactory receptor proteins in vertebrates and most other phyla (except insects which use ligand-gated channels) •Odorants bind to 7-helix (G-protein coupled) receptors. •In mice, >1000 genes (2-3% of genes!) encode these receptors. •Humans have about 350 odorant receptors •Receptor sequences also are quite variable, especially in putative odorant-binding helices. •Thus, the repertoire is extremely diverse. •In mammals, each neuron probably expresses only a single receptor. 6 •Odorant binding and signal transduction occurs in the cilia (top left) •Amino-acid sequences of odorant receptors are highly variable (black dots indicate most variable residues) (bottom left) •Odorant binding to GPCR triggers a cascade that opens a cAMP-gated cation channel (right) 7 Olfactory neurons have cAMP-activated Na+/Ca2+ Channels receptor G protein i q s t effector channel enzyme Excised “inside-out” patch allows access to the inside surface of the membrane +cAMP intracellular messenger cAMP Ca2+ cGMP channel no cAMP no channel openings open +cAMP closed 8 More about olfactory channels and their role in olfactory transduction Olfactory cAMP-gated channels are permeable to Na+ and Ca2+ Thus, odorant binding causes depolarization of the olfactory neuron through Na+ entry. Ca2+ also enters and activates a Cl - channel, increasing depolarization (ECl is near zero in these cells). This process stimulates the olfactory neuron to fire action potentials. 9 Olfactory bulb Olfactory epithelium Expression zones of 4 individual olfactory receptors (rat nose, coronal section) Olfactory receptor K20 The olfactory turbinates display four ‘expression zones’. Each receptor is expressed in a small, randomly K21 distributed subset of neurons within one of the 4 zones . As there are ~1000 receptors, about 4-5 neurons within L45 a zone express each receptor. A16 Neurons within each expression zone send axons to a different quadrant of the olfactory bulb. Another gene class, expressed in all olfactory neurons Figure 32-5 10 Projections to the olfactory bulb To lateral olfactory tract Olfactory neurons send axons to the glomeruli (synaptic balls shielded by glia) of the olfactory bulb. Olfactory neurons excite mitral cells, which are the bulb glomus, ball of yarn (Latin) output cells. like a bishop’s miter (hat) Inhibitory Mitral cell Tufted cell Periglomerular cell perforated (Latin) Olfactory sensory neuron Figures 32-1, 32-6 11 Each glomeruli receives inputs from sensory neurons expressing the same odorant receptor Neurons expressing a specific olfactory receptor project their axons to a single glomerulus in each half-bulb. Axons converge from many directions onto the target. This projection specificity is at least partly determined by the receptor itself, but the mechanisms are unknown. 12 Mapping glomerular odorant responses: Ca2+ imaging in a fish Individual glomeruli are selectively activated by specific odorants. In fish, “odorants” are soluble amino acids. Imaging studies now show that specific glomeruli in mammals are also activated in response to odorants. 13 Maps of mitral cell projections to higher olfactory areas Piriform cortex neurons receive projections from mitral cells corresponding to many glomeruli that receive input from ORNs expressing different receptors. Mitral cells also project to olfactory tubercle and other areas. Integration of odorant responses and odorant identification may take place in cortex, although some integration is also likely to occur in the bulb. 14 The vomeronasal organ The VNO is thought to respond to pheromones. It is a cup-shaped organ near the front of the rodent nose; its neurons are divided into basal and apical (near the lumen) layers. The microvilli of the VNO neurons face the lumen. Neurons in the apical layer express the G protein α subunit Gαi2, while those in the basal layer express Gαo. The transduction channel and the receptors are located on the microvilli at the edge of the lumen. 15 VNO receptor molecules The 2 distinct families of VNO G protein-coupled receptors are all unrelated to MOE receptors. Each VNO neuron probably expresses only one odorant receptor, as in the MOE. V1Rs (~180 genes) are expressed by V2Rs (~100 genes in the rodent) are different subsets of neurons within the expressed in a random pattern by basal layer apical layer (Gi-expressing neurons). neurons (Go-expressing neurons). V2Rs have large N-terminal extracellular domains. Figure 32-9 16 The GPCR pathway in a VNO cell resembles the Gq pathway receptor G protein i q s t effector channel enzyme intracellular messenger Ca2+ cAMP cGMP IP3 DAG channel 17 (like the GPCR lecture) VNO signal transduction TRPC2 channel phosphatidyl inositol 4,5 bisphosphate = PI(4,5)P2 Like Alberts 15-36 © Garland 18 Response characteristics of VNO neurons VNO neurons respond to urine. Some neurons selectively respond to urine from mice of the same sex, others to urine of the opposite sex. Unlike ORNs, their responses are narrowly tuned; no neurons were ever observed to respond to more than one compound. A behavioral assay: mice produce ultrasonic calls (‘whistling’) in response to contact with urine from the opposite sex; production of these calls requires both the VNO and the MOE. In TRPC2 knockout mice, VNO neurons do not respond to urine; and mice do not vocalize in response to urine 19 Acessory olfactory bulb (AOB) projections to the brain Mitral cells in the AOB have apical dendrites that arborize in multiple glomeruli. The AOB projects to the amygdala (directly), and the hypothalamus (via the amygdala). The projections from the rostral and caudal AOB halves are superimposed in the amygdala. This implies that integration of pheromone signals may take place primarily in the AOB. 20 Odorant perception by the vomeronasal system is largely unconscious The main olfactory system mediates cortical responses to volatile odorants, and these cortical responses are used to drive conscious behavior (foodseeking, predator avoidance, etc). The VN system is thought to mediate unconscious responses to water-soluble pheromone compounds found in urine and secretions of other individuals. 21 Chemical composition of pheromones The various pheromones include prostaglandins in fish, androstenone in pigs, and protein ligands such as hamster aphrodisin. In most cases, however, individual pure compounds don’t elicit strong responses. Natural pheromones are mixtures of many substances, perhaps combinations of (protein carriers) plus (bound small organic compounds). 22 End of Lecture 16 23