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The Olfactory System and Its Disorders

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The Olfactory System and Its Disorders The Olfactory System and Its Disorders Richard L. Doty, Ph.D.1 ABSTRACT The sense of smell is greatly underappreciated, despite the fact that it monitors the intake of airborne agents into the human respiratory system and determines to a large degree the flavor and palatability of foods and beverages. In addition to enhancing quality of life, this primary sensory system warns of spoiled foods, leaking natural gas, polluted air and smoke, and mediates basic elements of communication (e.g., mother–infant interactions). It is now apparent that smell dysfunction is among the first clinical signs of such neurodegenerative diseases as Alzheimer’s disease and sporadic Parkinson’s disease. In this brief article, the author reviews the anatomy and physiology of this primary sensory system, means of assessing its function, and major diseases and disorders with which it is intimately associated. KEYWORDS: Smell, olfaction, anosmia, dysosmia, Alzheimer’s disease, Parkinson’s disease, aging Although neglected by the medical community enter the nasal pharynx during deglutition.9 These at large, olfaction is critically important for safety, nutri- sensations disappear when the olfactory epithelium is tional status, and quality of life; its dysfunction is now markedly damaged, leaving intact only somatosensory known to be among the earliest ‘‘preclinical’’ signs of sensations and the perception of the primary taste qual- Alzheimer’s disease (AD) and sporadic Parkinson’s dis- ities of sweet, sour, salty, bitter, metallic, and umami ease (PD).1–6 Among 750 consecutive patients present- (monosodium glutamate–like). Whole-mouth taste func- ing to the University of Pennsylvania Smell and Taste tion is much more resilient to pathologic or trauma- Center with chemosensory complaints, 68% experienced related alterations than is smell function, in large part an altered quality of life, 46% changes in appetite or because of the redundant innervation of the taste buds body weight, and 56% adverse influences on daily from several cranial nerves (i.e., CN VII, IX, and X).7 living or psychological well-being.7 In another study of In this article the anatomy and physiology of the 445 patients with complaints of chemosensory disturb- olfactory system is reviewed, as well as means for assess- ance, at least one hazardous event, such as food poison- ing its function and disorders in which it is intimately ing or failure to detect fire or leaking natural gas, was involved. Emphasis is placed on disorders commonly reported by 45.2% of those with anosmia, 34.1% of those encountered by the practicing neurologist. with severe hyposmia, 32.8% of those with moderate hyposmia, 24.2% of those with mild hyposmia, and This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited. 19.0% of those with normal olfactory function.8 ANATOMY AND PHYSIOLOGY Most complaints of decreased ‘‘taste’’ function actually reflect decreased smell function.7 Such flavors Sensory Receptors and Primary Neurons as coffee, chocolate, vanilla, strawberry, pizza, licorice, The peripheral elements of the olfactory system consist steak sauce, root beer, and cola are dependent upon of 6 million bipolar receptor cells whose cell bodies, stimulation of cranial nerve (CN) I from volatiles that dendrites, and initial axon segments are located within 1Smell and Taste Center, University of Pennsylvania School of Disorders of the Cranial Nerves; Guest Editor, William W. Campbell, Medicine, Philadelphia, Pennsylvania. M.D., M.S.H.A. Address for correspondence and reprint requests: Richard L. Doty, Semin Neurol 2009;29:74–81. Copyright # 2009 by Thieme Ph.D., Professor and Director, Smell and Taste Center, University of Medical Publishers, Inc., 333 Seventh Avenue, New York, NY Pennsylvania School of Medicine, 5 Ravdin Pavilion, 3400 Spruce 10001, USA. Tel: +1(212) 584-4662. Street, Philadelphia, PA 19104 (e-mail: [email protected]). DOI 10.1055/s-0028-1124025. ISSN 0271-8235. 74 THE OLFACTORY SYSTEM AND ITS DISORDERS/DOTY 75 the olfactory neuroepithelium in the roof of the nasal ify and degrade odorants, and transport some molecules chamber.10 This pseudostratified columnar epithelium is across the epithelium. However, most of the mucus that supported by a highly vascularized lamina propria cover- covers the surface of the olfactory epithelium comes from ing the cribriform plate, the superior septum, and sectors Bowman’s glands, specialized glands found only within of both the superior and middle turbinates.11 The the olfactory epithelium. Among other cell types within receptor cell axons project through the cribriform plate this epithelium are basal stem cells (the precursors of all of the ethmoid bone and synapse within the glomerular of the main types of cells of the epithelium) and the layer of the olfactory bulb after forming into bundles— poorly understood microvillar cells, which number the olfactory fila. Receptor-bearing cilia, numbering 600,000 in humans and send tufts of microvilli into from 3 to 50 per cell, project from the dendritic ends the nasal mucus.10 of the receptor cells into the overlying mucus, in some cases radiating over 30 mm. In the human, the surface area of the cilia is 25 mm2.12 Olfactory Bulbs and Their Projections The bipolar receptor neurons are unique in several Each ovoid olfactory bulb is located at the base of the ways. First, they can regenerate from basal cells after frontal lobe overlying the cribriform plate of the ethmoid being damaged. Second, each cell serves as both a bone. The olfactory bulbs are composed of neurons, receptor cell and a first-order neuron, projecting an afferent and efferent nerve fibers, multiple interneurons, axon directly from the nasal cavity into the brain without microglia, astrocytes, and blood vessels, all surrounded an intervening synapse. Their rather direct exposure to by a thin layer of pia-arachnoid cells.19 The bulb’s the external environment, along with their large surface cellular elements are arranged in six concentric layers: area and minimal xenobiotic-metabolizing capacity, the olfactory nerve layer, the glomerular layer, the make them a primary route of invasion into the brain external plexiform layer, the mitral cell layer, the internal of several xenobiotic agents. Indeed, many neurovirulent plexiform layer, and the granule cell layer. The latter viruses are capable of penetrating the brain via the layer makes up about half the volume of the entire bulb. olfactory receptor cells.13 Finally, such cells are highly The receptor cell axons synapse within the spher- specialized, individually expressing receptors that re- ical olfactory bulb glomeruli, which are arranged in spond to only certain elements of odorant ligands.14 single or double layers. These structures number in the The initial step in olfactory transduction is the thousands in younger persons and are a defining feature movement of odorants from the air phase of the nasal of the olfactory system. With age, however, the number cavity into the aqueous phase of the olfactory mucus. and integrity of the glomeruli greatly decrease, being Odorants, most of which are hydrophobic, then diffuse nearly absent in elderly persons.20 The development and or are transported through the aqueous medium to maintenance of the glomeruli depend on trophic influ- olfactory receptor proteins of the cilia, ultimately induc- ences exerted by the receptor cells. Because a given ing action potentials in the receptor cells.15 Although receptor cell projects to only one or two glomeruli, the several odorants stimulate free nerve endings from CN V glomeruli are, in effect, functional representations of the and some other cranial nerves distributed in the nasal receptor types.14 mucosa, nasal pharynx, or oral cavity, such stimulation The main second-order neurons, which are the primarily involves somatosensory sensations of the primary output neurons of the bulb, are the mitral and ‘‘common chemical sense,’’ such as warmth, coolness, tufted cells. The apical dendrites of these cells are pungency, and irritation.16 influenced not only by the olfactory nerve terminals, There is marked genetic diversity in olfactory but also by interneurons and centrifugal fibers, most of receptors. A large multigene rodent family of 1000 which are GABAergic or dopaminergic.21 Several bulbar genes appears to code for odorant receptor proteins with interneurons, including the granule cells, are replaced by This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited. seven transmembrane domains.17 In humans, more than progenitors germinating within the subventricular zone half of this receptor gene family are pseudogenes, of the brain. These cells migrate along the rostral indicating that the number of functional receptors is migratory stream to the olfactory bulb.22 less than 500.18 Even though each receptor cell expresses only one type of olfactory receptor, such cells respond to a wide range of odorants. However, a given receptor, Olfactory Cortex though a ‘‘generalist,’’ does not respond to all stimuli The mitral and tufted cell axons leave the bulb via the to which another receptor responds, thereby allowing for lateral olfactory tract to synapse on structures collectively cross-neuron quality coding.14 termed the primary olfactory cortex, including the ante- The olfactory receptors cells are physically iso- rior olfactory nucleus (AON), the piriform cortex, the lated from one another within the olfactory neuroepi- anterior cortical
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