Information processing in mammalian olfactory system

In recent years, considerable progress has been made in understanding how the olfactory system uses neural space to encode sensory information. In this review, we focus on recent studies aimed at understanding the organizational strategies used by the mammalian olfactory system to encode information. The odorant receptor gene family is discussed in the context of its genomic organization as well as the specificity of olfactory sensory neurons. These data have important consequences for the mechanisms of odorant receptor gene choice by a given sensory neuron. Division of the olfactory epithelium into zones that express different sets of odorant receptors is the first level of input organization. The topographical relationship between periphery and olfactory bulb represents a further level of processing of information and results in the formation of a highly organized spatial map of information in the olfactory bulb. There, local circuitry refines the sensory input through various lateral interactions. Finally, the factors that may drive the development of such a spatial map are discussed. The onset of expression and the establishment of the zonal organization of odorant receptor genes in the epithelium are not dependent upon the presence of the olfactory bulb, suggesting that the functional identity of olfactory sensory neurons is determined independently of target selection. © 1996 John Wiley & Sons, Inc.     

Neuronal degeneration and regeneration in the olfactory epithelium of pigeon following transection of the first cranial nerve.

The pigeon olfactory nerve has been sectioned to explore the course of retrograde degeneration of the sensory neurons' perikarya, which are located in the olfactory neuroepithelium. Both light- and electron-microscopic observations have shown that from 3 to 8 days after axotomy the sensory neurons undergo retrograde, irreversible degeneration. Following disappearance of the mature neurons, the basal cells of the neuroepithelium actively divide and differentiate into mature olfactory sensory neurons. Consequently, the basal cells represent true stem cells of the olfactory sensory neurons. The olfactory mucosa regains a structural organization close to normal in a period of 30-50 days after axotomy. These observations indicate that, when the primary olfactory neurons degenerate as a consequence of the experimental section of their axons, restitutio ad integrum of the sensory olfactory connections can be reestablished by new elements which differentiate from basal cells of the olfactory neuroepithelium.20     

The ultrastructural organization of olfactory epithelium of two species of gadoid fish

The untrastructural organization of the olfactory epithelium of the cod Gadus morhua (L.) and the haddock Melanogrammus aeglefinus (L.) was studied using both transmission and scanning electron microscopy. The olfactory rosette was found to exhibit regional differences; the faces of the olfactory lamella were composed of sensory epithelium, the edges were non-sensory. The cellular organization of the olfactory epithelium was determined and consisted of bi-polar sensory neurones, supporting cells, mucous cells and basal cells. The ultrastructure of the sensory cells was consistent, having an elongate cell, the free surface of which terminated in an olfactory vesicle from which arose either four olfactory cilia or numerous microvilli. Ciliary aggregations have been found in the two species of gadoid fish studied; it is suggested that these structures aid in the separation and in the circulation of fluid between the lamellae. The surface structure of the supporting cells was found to be of two types: either ciliated or ridged; the former presenting distinct ciliated tufts, the latter showing definite, but unorganized, ridges over the epithelium surface.     

A map of pheromone receptor activation in the mammalian brain

In mammals, the detection of pheromones is mediated by the vomeronasal system. We have employed gene targeting to visualize the pattern of projections of axons from vomeronasal sensory neurons in the accessory olfactory bulb. Neurons expressing a specific receptor project to multiple glomeruli that reside within spatially restricted domains. The formation of this sensory map in the accessory olfactory bulb and the survival of vomeronasal organ sensory neurons require the expression of pheromone receptors. In addition, we observe individual glomeruli in the accessory olfactory bulb that receive input from more than one type of sensory neuron. These observations indicate that the organization of the vomeronasal sensory afferents is dramatically different from that of the main olfactory system, and these differences have important implications for the logic of olfactory coding in the vomeronasal organ.     

Zonal organization of the mammalian main and accessory olfactory systems

Zonal organization is one of the characteristic features observed in both main and accessory olfactory systems. In the main olfactory system, most of the odorant receptors are classified into four groups according to their zonal expression patterns in the olfactory epithelium. Each group of odorant receptors is expressed by sensory neurons distributed within one of four circumscribed zones. Olfactory sensory neurons in a given zone of the epithelium project their axons to the glomeruli in a corresponding zone of the main olfactory bulb. Glomeruli in the same zone tend to represent similar odorant receptors having similar tuning specificity to odorants. Vomeronasal receptors (or pheromone receptors) are classified into two groups in the accessory olfactory system. Each group of receptors is expressed by vomeronasal sensory neurons in either the apical or basal zone of the vomeronasal epithelium. Sensory neurons in the apical zone project their axons to the rostral zone of the accessory olfactory bulb and form synaptic connections with mitral tufted cells belonging to the rostral zone. Signals originated from basal zone sensory neurons are sent to mitral tufted cells in the caudal zone of the accessory olfactory bulb. We discuss functional implications of the zonal organization in both main and accessory olfactory systems.     

Morphology and histochemistry of the peripheral olfactory organ in the round goby,Neogobius melanostomus (Teleostei: Gobiidae)

This first comprehensive study of the peripheral olfactory organ from a representative of the large and economically important order of teleost fishes, the Perciformes, shows a compact structure with olfactory sensory neurons distributed widely throughout the olfactory chamber. The spatial organization of the nasal cavity in the bottom-dwelling round goby (Gobiidae, Neogobius melanostomus) was examined using impression material injection, immunocytochemistry, and transmission electron microscopy. The olfactory chamber contains a single olfactory lamella; prominent dorsocaudal lachrymal and ethmoidal accessory nasal sacs are situated ventrocaudal to the chamber. The location of the olfactory mucosa within the olfactory chamber is novel for teleost fish, as it extends beyond the ventral surface to the lateral and dorsal regions. Microvillar olfactory sensory neurons and ciliated olfactory sensory neurons were identified by transmission electron microscopy and the spatial distribution of these two cell types was assessed through immunocytochemistry against olfactory receptor coupled G-proteins. Both G(alphaolf)-immunoreactive ciliated olfactory sensory neurons and the G(alphao)-immunoreactive microvillar form were located throughout the olfactory epithelium. Ciliated crypt cells were G(alphao) immunoreactive and were found throughout the olfactory epithelium of some specimens. The widespread occurrence of olfactory sensory neurons in the olfactory chamber supports the idea that olfactory signaling is important to the survival of the round goby. The prominence of the lachrymal and ethmoidal accessory nasal sacs indicates the capacity to regulate the flow of odorant molecules over the sensory surface of the olfactory sensory neurons, possibly through a pump-like mechanism driven by opercular activity associated with gill ventilation.     

Organization of the olfactory system of the Indian major carp <Emphasis Type="Italic">Labeo rohita</Emphasis> (Ham.): A scanning and transmission electron microscopy study

Catla catla, Labeo rohita, and Cirrhinus mrigala represent important alimentary fish in India. Their reproduction/breeding depends on seasons. Fish perceive external factors-stimuli and chemical signals through the olfactory system that plays the key role in central regulation of reproduction. However, no electron microscopy data are available on organization of olfactory components of these fish. We studied organization of the olfactory organ in male L. rohita using scanning (SEM) and transmission electron microscopy (TEM). This organ consists of olfactory epithelium, a short nerve, and olfactory bulb. The olfactory organ is ovoid in shape and consists of about 47–52 lamellae in adults and about 14–20 lamellae in fingerlings. These lamellae originate from the midline raphe. By SEM, microvillar sensory and ciliated non-sensory cells were observed in the lamellae. TEM revealed microvillar receptor cell with rough endoplasmic reticulum and Golgi apparatus towards apical end. Basal cells were present at the base of receptor cell, supporting cells were located adjacent to the olfactory receptor neurons, while epithelial cells—in the nonsensory part of olfactory epithelium. Mast, blastema, and macrophage cells were also found at the basement membrane. This work is the first publication on ultrastructural organization of the olfactory system of the Indian major carp, which provides information about morphological and ultrastructural organization of the olfactory system and opens new avenues for further investigation of chemical neuroanatomy, sensory signal processing, and neural regulation of reproduction in the Indian major carp.     

Chemosensory-induced motor behaviors in fish

Chemical sensory signals play a crucial role in eliciting motor behaviors. We now review the different motor behaviors induced by chemosensory stimuli in fish as well as their neural substrate. A great deal of research has focused on migratory, reproductive, foraging, and escape behaviors but it is only recently that the molecules mediating these chemotactic responses have become well-characterized. Chemotactic responses are mediated by three sensory systems: olfactory, gustatory, and diffuse chemosensory. The olfactory sensory neuron responses to chemicals are now better understood. In addition, the olfactory projections to the central nervous system were recently shown to display an odotopic organization in the forebrain. Moreover, a specific downward projection underlying motor responses to olfactory inputs was recently described.     

Organization of olfactory system of the Indian major carp Labeo rohita (Ham.): a study using scanning and transmission microscopy

Catla catla, Labeo rohita, and Cirrhinus mrigala are important alimentary fish in India. Their reproduction (breeding) depends on season. The fish perceive external factors-stimuli and chemical signals through the olfactory system that plays the key role in the central regulation of reproduction. However, in the available literature, any electron microscopy data on organization of olfactory elements in these fish are absent. We have studied ultrastructure of the olfactory organ in male L. rohita by using scanning (SEM) and transmission electron microscopy (TEM). The olfactory organ consists of olfactory epithelium, a short nerve, and olfactory bulb. The organ has oval shape and consists of approximately 47-52 lamellae in adult fish and of 14-20 lamellae in fish at the stage of fingerling. These lamellae originate from the midline raphe. By using SEM, the presence of microvillar sensory and ciliated non-sensory cells in these lamellae is shown. By using TEM, a microvillar receptor cell is revealed, which has rough endoplasmic reticulum and Golgi apparatus towards the apical end. Basal cells are found at the base of the receptor cell; supporting cells are located adjacent to olfactory receptor neurons, while epithelial cells--in the non-sensory part of olfactory epithelium. Mast, blastema and macrophages cells are also found in the basal lamina. This work is the first publication on structural organization of olfactory system of the Indian major carp, which provides information about morphological and ultrastructural organization of olfactory system and opens new opportunities for study of chemical neuroanatomy, sensory signal processing, and nervous regulation of reproduction of the Indian major carp.     

Silence sets on a sensory map

Recent efforts to understand the contribution of neuronal activity in the creation of the olfactory sensory map have focused on odor-evoked events. In this issue of Neuron, Yu et al. discover a new role for neuronal activity in the organization and maintenance of the olfactory system. Their results highlight the role of spontaneous activity and synaptic transmission in axon outgrowth and olfactory neuron survival.     

Olfactory receptor gene expression

Recognition and discrimination of odorous molecules are determined by heptahelical G-protein-coupled receptor proteins localized primarily in the ciliary membrane of olfactory sensory neurons. The discovery of a large multigene family encoding odorant receptors allows us to approach various facets concerning the molecular basis of olfactory chemospecificity, ranging from chromosomal localization and control of expression of olfactory receptor genes to temporal and spatial expression patterns of various receptor types in the nasal neuroepithelium. The target-independent onset of receptor expression and its topographical organization suggest a precommited functional identity of olfactory neurons.     

Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius)

Summary The olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) has been studied with a conventional histochemical and a novel immunological staining technique. In both species, the sensory epithelium is arranged in folds separated by non-sensory epithelial tissue. In the nine-spined stickleback, intrinsic folds consisting of non-sensory cells are found in the apical part of the sensory epithelium where they divide the surface of the sensory epithelium into small islets. These non-sensory cells are non-ciliated, flattened and piled on top of each other; they contain numerous electron-translucent vesicles. The intrinsic folds are absent from the sensory epithelium of the three-spined stickleback. In both species, axons of receptor cells form a layer of fibers in the sensory epithelium immediately above the basal cells. In the three-spined stickleback, thick branches of the olfactory nerve are frequently found in this layer. These branches are only occasionally observed in the sensory epithelium of the nine-spined stickleback. Thus, the three-spined stickleback and the nine-spined stickleback show considerable differences in the organization of the sensory regions of the olfactory epithelium.     

Olfaction in zebrafish: what does a tiny teleost tell us?

Zebrafish, Danio rerio, possess a well-developed sense of smell which governs a variety of behaviors. Both the number of odorant receptor genes and the number of modules in the olfactory bulb (glomeruli) are about an order of magnitude smaller than those of mammals. Nevertheless, the spatial organization of functional properties within the sensory surface and the olfactory bulb are comparable to those of mammals. The quantitatively reduced olfactory system of zebrafish, together with the suitability of this species for developmental and genetic studies, make zebrafish an interesting model system to study olfactory differentiation and neuronal representation of olfactory information.     

Surface structure of the olfactory organ of marine teleosts

By means of the electron scanning microscope, structure of the olfactory rosella has been investigated in 5 species of marine Teleostei. Among the species investigated variability in number and arrangement is observed in the olfactory rosella folds. Arrangement order of the receptor and indifferent epithelia of the fold is presented by four types. Interspecies differences in organization of the sensory epithelium is revealed in ratio of various types of receptor and secretory cells. In Teleostei flagellar olfactory cells are the most numerous. In the Limanda yokohamae sensory epithelium certain flagella are described, that essentially differ by their size from usual receptor flagella and, evidently, are their complexes. The secretory cells are found in indifferent and sometimes in sensory epithelium as dark ostia; they are most numerous in mediosmatics. Some of the ostia are like wide craters and are, evidently, ostia of ducts of multicellular olfactory glands.     

All in a sniff: olfaction as a model for active sensing

Sensation is an active process involving the sampling and central processing of external stimuli selectively in space and time. Olfaction in particular depends strongly on active sensing due to the fact that-at least in mammals-inhalation of air into the nasal cavity is required for odor detection. This seemingly simple first step in odor sensation profoundly shapes nearly all aspects of olfactory system function, from the distribution of odorant receptors to the functional organization of central processing to the perception of odors. The dependence of olfaction on inhalation also allows for profound modulation of olfactory processing by changes in odor sampling strategies in coordination with attentional state and sensory demands. This review discusses the role of active sensing in shaping olfactory system function at multiple levels and draws parallels with other sensory modalities to highlight the importance of an active sensing perspective in understanding how sensory systems work in the behaving animal.     

Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing

The continued addition of new neurons to mature olfactory circuits represents a remarkable mode of cellular and structural brain plasticity. However, the anatomical configuration of newly established circuits, the types and numbers of neurons that form new synaptic connections, and the effect of sensory experience on synaptic connectivity in the olfactory bulb remain poorly understood. Using in vivo electroporation and monosynaptic tracing, we show that postnatal-born granule cells form synaptic connections with centrifugal inputs and mitral/tufted cells in the mouse olfactory bulb. In addition, newly born granule cells receive extensive input from local inhibitory short axon cells, a poorly understood cell population. The connectivity of short axon cells shows clustered organization, and their synaptic input onto newborn granule cells dramatically and selectively expands with odor stimulation. Our findings suggest that sensory experience promotes the synaptic integration of new neurons into cell type-specific olfactory circuits.     

Stability,variability, and parallelisms in the development of distant sensory systems: Olfactory and visual systems in the phylogeny and ontogeny of gastropods

The results of studies in the field of olfactory and visual systems of a number of gastropod representatives, differing in the general level of organization, phylogenetic position, habitat, and mode of life are given. The direction, general patterns, features, and parallels in the development of these sensory structures and related integrative brain regions in different phylogenetic lineages of gastropods are traced. Parallels in the development of the olfactory system of mollusks, insects, and vertebrates are shown. The important role of the habitat and mode of life of animals in the formation of specific patterns of evolutionary development of sensory organs is noted.     

Interchromosomal interactions and olfactory receptor choice

The expression of a single odorant receptor (OR) gene from a large gene family in individual sensory neurons is an essential feature of the organization and function of the olfactory system. We have used chromosome conformation capture to demonstrate the specific association of an enhancer element, H, on chromosome 14 with multiple OR gene promoters on different chromosomes. DNA and RNA fluorescence in situ hybridization (FISH) experiments allow us to visualize the colocalization of the H enhancer with the single OR allele that is transcribed in a sensory neuron. In transgenic mice bearing additional H elements, sensory neurons that express OR pseudogenes also express a second functional receptor. These data suggest a model of receptor choice in which a single trans-acting enhancer element may allow the stochastic activation of only one OR allele in an olfactory sensory neuron.     

Gross morphology and histology of the olfactory organ of the Greenland shark <Emphasis Type="Italic">Somniosus microcephalus</Emphasis>

The Greenland shark (Somniosus microcephalus) is the largest predatory fish in Arctic waters. Knowledge of the fundamental biology and ecological role of the Greenland shark is limited, and the sensory biology of the Greenland shark has been poorly studied. Given the potential relevant contribution of chemoreception to the sensory capability of the Greenland shark to forage and navigate in low-light environments, we examined the architecture of the peripheral olfactory organ (the olfactory rosette) through morphological, histological and immunohistochemical assays. We found that each olfactory rosette consists of a small number of lamellae (22) associated with a relatively high surface area of the olfactory epithelium. The general organization of the epithelium is similar to that described for other elasmobranchs. However, details that have emerged concerning the cell type composition (absence of crypt neurons, presence of unusually large cells along the olfactory fiber bundles) deserve further investigation. Overall, the structure of the olfactory rosette suggests a well-developed olfactory capability for the Greenland shark coherent with a bentho-pelagic lifestyle.     

Ultrastructure of the nuchal organ in the interstitial polychaete Stygocapitella subterranea (Parergodrilidae)

The nuchal organs of Stygocapitella subterranea are paired narrow pits. They are lined by unciliated cells at the opening and by ciliated cells at the basal parts. The primary sensory cells (6–8) are arranged in a single patch at the bottom of the nuchal pit. The nuclei of the sensory cells are located in the posterior portion of the brain. Their dendrites form the nuchal nerve which is sheathed by the ciliated cells. Each sensory cell bears up to 4 modified sensory cilia and several microvilli extending into the olfactory chamber. The sensory cilia show various patterns of axonemal organization and have no rootlets. The olfactory chamber is covered by a cuticular matrix. Another primary sensory cell lies at the opening of the nuchal pit. It bears cilia which penetrate the cuticle but are enveloped by the epicuticle. Retractor muscles insert caudally on the organ. The nuchal organ of S. subterranea shows similarities to those of opheliids but exhibits several features not to be found in other nuchal organs.