Thomas A. Schoenfeld

The anatomical logic of smell

Olfactory receptor neurons (ORNs) expressing the same odorant receptor gene share ligand-receptor affinity profiles and converge onto common glomerular targets in the brain. The activation patterns of different ORN populations, evoked by differential binding of odorant molecular moieties, constitute the primary odor representation. However, odorants possess properties other than receptor-binding sites that can contribute to odorant discrimination. Among terrestrial vertebrates, odorant sorptiveness--volatility and water solubility--imposes physicochemical constraints on migration through the nose during inspiration. The non-uniform distributions of ORN populations along the inspiratory axis enable sorptiveness to modify odor representations by affecting the number of molecules reaching different receptors during a sniff. Animals can then modify and analyze odor representation further by the dynamic regulation of sniffing.

The spatial organization of the peripheral olfactory system of the hamster. part I: Receptor neuron projections to the main olfactory bulb

The spatial organization of projections from olfactory receptor neurons to the main olfactory bulb (MOB) was studied in hamsters by using fluorescent stilbene isothiocyanates as retrograde tracers. Injections confined to small sectors of the MOB produce labeling of receptor neurons that is more restricted circumferentially (i.e., with respect to the medial-lateral and dorsal-ventral axes) than longitudinally (i.e., with respect to the rostral-caudal axis) along the mucosal sheet. This restricted labeling is also discontinuous, giving an initial impression that the peripheral input is only crudely organized with respect to the medial-lateral and dorsal-ventral axes of the nasal cavity. However, from analyses of serial sections, it is apparent that each set of mucosal segments shares convergent projections to a circumferential quadrant of the MOB with other segments that are positioned around a common domain of the nasal cavity airspace. The primary afferent projections to the MOB, thus, are organized rhinotopically (i.e., with respect to the three-dimensional position of receptor neurons in olfactory space) rather than mucosotopically.

Behavioral Development in the Syrian Golden Hamster

Study of behavioral development in hamsters had its formal beginnings in German ethology in the work of Dieterlen, Eibl-Eibesfeldt, and others. These studies offered some of the first descriptions of hamster pup behavior and established an important precedent for experimental inquiries into developmental mechanisms by the use of hamsters reared in isolation—the so-called Kaspar-Hauser animals (Dieterlen, 1959)—to test the importance of environmental stimuli on behavioral development.

The spatial organization of the peripheral olfactory system of the hamster. Part II: Receptor surfaces and odorant passageways within the nasal cavity

The spatial organization of olfactory receptor surfaces and odorant passageways within the nasal cavity was studied in hamsters through descriptive and morphometric analyses of a complete stereotaxically defined series of coronal, sagittal, and horizontal sections through the snout. These analyses reveal that the caudal two-thirds of each cavity is divided into two longitudinally oriented medial and lateral channels. The olfactory mucosa that lines these two channels projects selectively onto the medial and lateral halves of the main olfactory bulb (MOB), respectively. Moreover, the ethmoturbinates of the caudal recesses create highly convoluted channels, lined by ventrally projecting mucosa, that lie ventral, lateral, and dorsal to a relatively smooth central channel lined by dorsally projecting mucosa. The rhinotopic map makes equivalent representations of medial and lateral olfactory space to the MOB but gives the smooth space lined by dorsally projecting mucosa a disproportionately larger representation on the MOB than the convoluted space lined by the more expansive ventrally projecting mucosa. Recent descriptions of the spatial distribution of probes for odorant receptor proteins conform closely to this organization, giving credence to the idea that rhinotopy is a basis for representing to the MOB the specific molecular features of odorant molecules.

Evidence for the disproportionate mapping of olfactory airspace onto the main olfactory bulb of the hamster

Olfactory receptor neurons (ORNs) project to the rodent main olfactory bulb (MOB) from spatially distinct air channels in the olfactory recesses of the nose. The relatively smooth central channels of the dorsal meatus map onto the dorsal MOB, whereas the highly convoluted peripheral channels of the ethmoid turbinates project to the ventral MOB. Medial and lateral components of each projection stream innervate the medial and lateral MOB, respectively. To ascertain whether such topography entails the disproportionate representation seen in other sensory maps, we used disector‐based stereological techniques in hamsters to estimate the number of ORNs associated with each channel in the nose and the number of their targets (glomeruli and mitral and tufted cells) in corresponding divisions of the MOB. Each circumferential half of the MOB (dorsal/ventral, medial/lateral) contained about 50% of the 3,100 glomeruli and about 50% of the 160,000 mitral and tufted cells per bulb. We found equivalent numbers of ORNs with dendritic knobs in the medial and lateral channels (4.5 million each). However, the central channels had only 2 million knobbed ORNs, whereas the peripheral channels had 7 million. Thus, there is a disproportionate mapping of the central‐peripheral axis of olfactory airspace onto the dorsal‐ventral axis of the MOB, encompassing a greater than threefold variation in the average convergence of ORNs onto MOB secondary neurons. We hypothesize that the disproportionate projections help to optimize chemospecific processing by compensating, with differing sensitivity, for significant variation in the distribution and concentration of odorant molecules along the olfactory air channels during sniffing. J. Comp. Neurol. 476:186–201, 2004.

NADPH diaphorase activity in olfactory receptor neurons and their axons conforms to a rhinotopically-distinct dorsal zone of the hamster nasal cavity and main olfactory bulb

NADPH diaphorase histochemical protocols were optimized for the histochemical labeling of olfactory receptor neurons (ORNs) in the nasal cavity and their axon terminals in glomeruli of the main olfactory bulb (MOB) in the Syrian hamster. This labeling was then used to map and quantify the spatial distribution of ORNs and their central projections. Diaphorase-positive ORNs were found to be rhinotopically restricted to dorsal-medially situated segments of sensory mucosa associated with central air channels in the nose, together constituting about 25% of the total receptor sheet. This topography closely resembles the zonal expression patterns of putative odorant receptor genes and cell surface glycoconjugates in the nose. Moreover, the projections of ORNs in the diaphorase-positive dorsal/central zone were found to expand onto the entire dorsal half of the MOB, consistent with spatial patterns discerned in retrograde tract-tracing studies. These boundaries indicate that dorsal/central zone ORNs project to a disproportionately larger region of the MOB than do those in the more ventral/peripheral zones. The demonstration of NADPH diaphorase activity in ORNs is inconsistent with the expression of the best-known NADPH-dependent enzymes, such as nitric oxide synthase (neuronal and endothelial isoforms) and NADPH cytochrome P450 oxidoreductase. Understanding the spatial patterning of histochemical labeling in ORNs should facilitate the biochemical identification of this diaphorase.

Substance P and Luteinizing Hormone-Releasing Hormone Levels in the Brain of the Male Golden Hamster Are Both Altered by Castration and Testosterone Replacement

The effects of castration and testosterone (T) replacement on levels of substance P (SP) and luteinizing hormone-releasing hormone (LHRH) were assessed in discrete areas of the male hamster brain. The animals were either castrated, castrated and given a chronically low or high dose of T by Silastic implant, or sham-operated. Brain tissues and trunk blood were collected 3 weeks after surgery. Plasma T levels were maintained within the normal range by the implants but at significantly lower or higher levels than the mean for sham-operated males. Levels of SP and LHRH were quantified in the olfactory bulbs, rostral basal forebrain, anterior hypothalamic and preoptic area, medial basal hypothalamic area, medial basal hypothalamic area and median eminence, and brain stem. In general, castration and T replacement effected opposite changes in levels of SP and LHRH. In the medial basal hypothalamic area and median eminence SP levels were found to be inversely related to the chronic T levels, whereas the LHRH levels were directly correlated. In the anterior hypothalamic and preoptic area, castration reduced levels of SP. Conversely, castration elevated levels of LHRH in this area. This inverse dynamic relationship between changing peptide levels was also observed in the rostral basal forebrain but not in the olfactory bulbs. In most of these forebrain regions, the dose-response curves for the experimental groups could not incorporate the peptide levels in the sham-operated control group. SP levels in the brain stem showed a monotonic inverse relationship to circulating T levels which did include the control group values.(ABSTRACT TRUNCATED AT 250 WORDS)