Forebrain projections of the pigeon olfactory bulb

The olfactory system of the pigeon (Columba livia) was examined. Our electrophysiological and experimental neuroanatomical (Fink-Heimer technique) data showed that axons from the olfactory bulb terminated in both sides of the forebrain. The cortex prepiriformis (olfactory cortex), the hyperstriatum ventrale and the lobus parolfactorius comprised the uncrossed terminal field. The crossed field included the paleostriatum primitivum and the caudal portion of the lobus parolfactorius, areas which were reached through the anterior commissure. In this report the relationships between areas that receive olfactory information and the possible roles that olfaction plays in the birds' behavior are discussed.     

Patterns in air pollution as model for the physical basis for olfactory navigation in pigeon homing

Spatial distribution and temporal variability of air pollution were used as a model to describe the stability and predictability of the distribution of airborne substances, postulated by some to be used by homing pigeons to navigate. If the man-made substances reflect the distributional characteristics of natural airborne substances, navigation based on airborne substances is unlikely to be possible.     

Expression of extracellular matrix molecules in the embryonic rat olfactory pathway

Primary olfactory neurons arise from placodal neuroepithelium that is separate from the neuroepithelial plate that forms the neural tube and crest. The axons of these neurons course along a stereotypical pathway and invade the rostral telencephalic vesicle where they induce the formation of the olfactory bulb. In the present study we examined the expression of several extracellular matrix constituents during formation of the olfactory nerve pathway in order to identify putative developmentally significant molecules. Double-label immunofluorescence was used to simultaneously map the trajectory of growing primary olfactory axons by expression of growth associated protein 43 (GAP-43) and the distribution of either laminin, heparan sulfate proteoglycans (HSPG), or chondroitin sulfate proteoglycans (CSPG). At embryonic day 12.5 (E12.5) primary olfactory axons have exited the olfactory neuroepithelium of the nasal pit and formed a rudimentary olfactory nerve. These axons together with migrating neural cells form a large mass outside the rostral surface of the telencephalon. This nerve pathway is clearly defined by a punctate distribution of laminin and HSPG. CSPG is selectively present in the mesenchyme between the olfactory nerve pathway and the nasal pit and in the marginal zone of the telencephalon. At E14.5 primary olfactory axons pierce the telencephalon through gaps that have emerged in the basement membrane. At this age both laminin and HSPG are colocalized with the primary olfactory axons that have entered the marginal zone of the telencephalon. CSPG expression becomes downregulated in this same region while it remains highly expressed in the marginal zone adjacent to the presumptive olfactory bulb. By E16.5 most of the basement membrane separating the olfactory nerve from the telencephalon has degraded, and there is direct continuity between the olfactory nerve pathway and the central nervous system. This strict spatiotemporal regulation of extracellular matrix constituents in the olfactory nerve pathway supports an important role of these molecules in axon guidance. We propose that laminin and HSPG are expressed by migrating olfactory Schwann cells in the developing olfactory nerve pathway and that these molecules provide a conducive substrate for axon growth between the olfactory neuroepithelium and the brain. CSPG in the surrounding mesenchyme may act to restrict axon growth to within this pathway. The regional degradation of the basement membrane of the telencephalon and the downregulation of CSPG within the marginal zone probably facilitates the passage of primary olfactory axons into the brain to form the presumptive nerve fiber layer of the olfactory bulb. © 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     

A dynamical feedback model for adaptation in the olfactory transduction pathway

Olfactory transduction exhibits two distinct types of adaptation, which we denote multipulse and step adaptation. In terms of measured transduction current, multipulse adaptation appears as a decrease in the amplitude of the second of two consecutive responses when the olfactory neuron is stimulated with two brief pulses. Step adaptation occurs in response to a sustained steplike stimulation and is characterized by a return to a steady-state current amplitude close to the prestimulus value, after a transient peak. In this article, we formulate a dynamical model of the olfactory transduction pathway, which includes the kinetics of the CNG channels, the concentration of Ca ions flowing through them, and the Ca-complexes responsible for the regulation. Based on this model, a common dynamical explanation for the two types of adaptation is suggested. We show that both forms of adaptation can be well described using different time constants for the kinetics of Ca ions (faster) and the kinetics of the feedback mechanisms (slower). The model is validated on experimental data collected in voltage-clamp conditions using different techniques and animal species.     

3H]-GABA selective retrograde labeling of neurons in the pigeon thalamo-Wulst pathway

Evidence is presented which is consistent with a specific retrograde labeling of GABAergic neurons following [3H]-GABA application in their zone of termination. [3H]-GABA injection in the pigeon Wulst leads to perikaryal retrograde labeling in the ipsilateral thalamic visual relay, n. dorsolateralis anterior thalami, pars lateralis (DLLv). This result gives further support to the biochemical evidence of the existence, in the pigeon, of a GABAergic projection from DLLv to the ipsilateral visual Wulst.     

Response properties of higher level neurons in the central olfactory pathway of the crayfish

We have examined the electrical activity of interneurons within the higher levels of the crayfish olfactory system. In unstimulated isolated crayfish head preparations, local protocerebral interneurons (LPI) of the hemiellipsoid bodies generate periodic, low-frequency membrane depolarizations. The most reasonable explanation for these baseline fluctuations, which were exhibited by all of the LPIs examined and which were reversibly abolished by either tetrodotoxin or low-calcium saline solution, is that they reflect periodic synaptic drive from the axon terminals of olfactory projection neurons. One-third of tested LPIs generated impulses in response to the odor stimuli we applied to the antennules. Those cells that did respond exhibited a brief excitatory postsynaptic potential and one or two action potentials, even during prolonged odor pulses. Many of the responding neurons also exhibited a delayed impulse burst 1 or 2 s following the stimulus pulse. Most of the responding cells recovered their sensitivity to odors very slowly, exhibiting disadaptation periods of several minutes. The apparent refractory nature of individual LPIs to olfactory stimulation is attributed in part to a hypothesized selectivity of connections between projection neurons and protocerebral targets and in part to the electrical isolation of the recording electrode from many regions of the extensive LPI dendritic tree. Accepted: 20 March 1997     

Lack of fibulin-3 alters regenerative tissue responses in the primary olfactory pathway

The adult olfactory epithelium has maintained the ability to reconstitute its olfactory sensory neurons (OSNs) from a basal progenitor cell compartment. This allows for life-long turnover and replacement of receptor components as well as repair of the primary olfactory pathway in response to injury and environmental insults. The present study investigated whether fibulin-3, a glycoprotein in the extracellular matrix and binding partner of tissue inhibitor of metalloproteinases-3 (TIMP-3), plays a role in ongoing plasticity and regenerative events in the adult primary olfactory pathway. In wild-type control mice, fibulin-3 protein was detected on IB4⁺CD31⁺ blood vessels, nerve fascicles and the basement membrane underneath the olfactory epithelium. After target ablation (olfactory bulbectomy), fibulin-3 was also abundantly present in the central nervous system (CNS) scar tissue that occupied the bulbar cavity. Using two different lesion models, i.e. intranasal Triton X-100 lesion and olfactory bulbectomy, we show that fibulin-3 deficient (Efemp1^?/?) mice have impaired recovery of the olfactory epithelium after injury. Ten days post-injury, Efemp1^?/? mice showed altered basal stem/progenitor cell proliferation and increased overall numbers of mature (olfactory marker protein (OMP) -positive) versus immature OSNs. However, compromised regenerative capacity of the primary olfactory pathway in Efemp1^?/? mice was evidenced by reduced numbers of mature OSNs at the later time point of 42 days post-injury. In addition to these neural differences there were consistent changes in blood vessel structure in the olfactory lamina propria of Efemp1^?/? mice. Overall, these data suggest a role for fibulin-3 in tissue maintenance and regeneration in the adult olfactory pathway.     

Mesenchymal/epithelial induction mediates olfactory pathway formation

In the olfactory pathway, as in the limbs, branchial arches, and heart, mesenchymal/epithelial induction, mediated by retinoic acid (RA), FGF8, sonic hedgehog (shh), and the BMPs, defines patterning, morphogenesis, and differentiation. Neuronal differentiation in the olfactory epithelium and directed growth of axons in the nascent olfactory nerve depend critically upon this inductive interaction. When RA, FGF8, shh, or BMP signaling is disrupted, distinct aspects of olfactory pathway patterning and differentiation are compromised. Thus, a cellular and molecular mechanism that facilitates musculoskeletal and vascular development elsewhere in the embryo has been adapted to guide the differentiation of the olfactory pathway in the developing forebrain.     

Effects of serotonin depletion on local interneurons in the developing olfactory pathway of lobsters

During embryonic life, the growth of the olfactory and accessory lobes of the lobster brain is retarded by serotonin depletion using 5,7-dihydroxytryptamine (5,7-DHT) (Benton et al., 1997). The local and projection interneurons that synapse with chemosensory cells in the olfactory lobes are potential targets of this depletion. This study documents proliferation and survival in the local interneuron cell clusters, and examines the differentiation of a prominent local interneuron, the serotonergic dorsal giant neuron (DGN), following serotonin depletion. An increase in dye coupling between the DGN and nearby cells is seen after serotonin depletion. However, morphometric analyses of individual DGNs in normal, sham-injected, and 5,7-DHT-treated embryos show that the general morphology and size of the DGNs are not significantly altered by serotonin depletion. Thus, the DGN axonal arbor occupies a greater proportion of the reduced olfactory lobes in the 5,7-DHT-treated embryos than in normal and sham-injected groups. The paired olfactory globular tract neutrophils (OGTNs), where olfactory interneurons synapse onto the DGNs, are 75% smaller in volume than the comparable region in either sham-injected or normal embryos. In vivo experiments using bromodeoxyuridine (BrdU) show that proliferation in the local interneuron soma clusters is reduced by 5,7-DHT treatment and that survival of newly proliferated local interneurons is also compromised. Our data suggest that alterations in the growth of the DGNs do not contribute to the dramatic reduction in size of the olfactory neutrophils following serotonin depletion, but that cell proliferation and survival among the local interneurons are regulated by serotonin during development. Reduced numbers of local interneurons are therefore one likely reason for the growth reduction observed after serotonin depletion.     

Ocean acidification alters foraging behaviour in Dungeness crab through impairment of the olfactory pathway

Crustacean olfaction is fundamental to most aspects of living and communicating in aquatic environments and more broadly, for individual- and population-level success. Accelerated ocean acidification from elevated CO₂ threatens the ability of crabs to detect and respond to important olfactory-related cues. Here, we demonstrate that the ecologically and economically important Dungeness crab (Metacarcinus magister) exhibits reduced olfactory-related antennular flicking responses to a food cue when exposed to near-future CO₂ levels, adding to the growing body of evidence of impaired crab behaviour. Underlying this altered behaviour, we find that crabs have lower olfactory nerve sensitivities (twofold reduction in antennular nerve activity) in response to a food cue when exposed to elevated CO₂. This suggests that near-future CO₂ levels will impact the threshold of detection of food by crabs. We also show that lower olfactory nerve sensitivity in elevated CO₂ is accompanied by a decrease in the olfactory sensory neuron (OSN) expression of a principal chemosensory receptor protein, ionotropic receptor 25a (IR25a) which is fundamental for odorant coding and olfactory signalling cascades. The OSNs also exhibit morphological changes in the form of decreased surface areas of their somata. This study provides the first evidence of the effects of high CO₂ levels at multiple levels of biological organization in marine crabs, linking physiological and cellular changes with whole animal behavioural responses.     

Dynamic expression of Pax6 in the shark olfactory system: evidence for the presence of Pax6 cells along the olfactory nerve pathway

Pax6 is involved in the control of neuronal specification, migration, and differentiation in the olfactory epithelium and in the generation of different interneuron subtypes in the olfactory bulb. Whether these roles are conserved during evolution is not known. Cartilaginous fish are extremely useful models for assessing the ancestral condition of brain organization because of their phylogenetic position. To shed light on the evolution of development of the olfactory system in vertebrates and on the involvement of Pax6 in this process, we analyzed by in situ hybridization and immunohistochemistry the expression pattern of Pax6 in the developing olfactory system in a basal vertebrate, the lesser spotted dogfish Scyliorhinus canicula. This small shark is becoming an important fish model in studies of vertebrate development. We report Pax6 expression in cells of the olfactory epithelium and olfactory bulb, and present the first evidence in vertebrates of strings of Pax6-expressing cells extending along the developing olfactory nerve. The results indicate the olfactory epithelium as the origin of these cells. These data are compatible with a role for Pax6 in the development of the olfactory epithelium and fibers, and provide a basis for future investigations into the mechanisms that regulate development of the olfactory system throughout evolution.     

Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway

Individual olfactory neurons in the antennal lobes of Periplaneta americana were investigated for their morphological and neurochemical properties by means of intracellular cobalt injection and indirect peroxidase-antiperoxidase immunohistochemistry. GABA-like immunoreactivity was demonstrated in many local interneurons but not in uniglomerular projection neurons.     

Dual olfactory pathway in Hymenoptera: evolutionary insights from comparative studies

In the honeybee (Apis mellifera) and carpenter ant (Camponotus floridanus) the antennal lobe output is connected to higher brain centers by a dual olfactory pathway. Two major sets of uniglomerular projection neurons innervate glomeruli from two antennal-lobe hemispheres and project via a medial and a lateral antennal-lobe protocerebral tract in opposite sequence to the mushroom bodies and lateral horn. Comparison across insects suggests that the lateral projection neuron tract represents a special feature of Hymenoptera. We hypothesize that this promotes advanced olfactory processing associated with chemical communication, orientation and social interactions. To test whether a dual olfactory pathway is restricted to social Hymenoptera, we labeled the antennal lobe output tracts in selected species using fluorescent tracing and confocal imaging. Our results show that a dual pathway from the antennal lobe to the mushroom bodies is present in social bees, basal and advanced ants, solitary wasps, and in one of two investigated species of sawflies. This indicates that a dual olfactory pathway is not restricted to social species and may have evolved in basal Hymenoptera. We suggest that associated advances in olfactory processing represent a preadaptation for life styles with high demands on olfactory discrimination like parasitoism, central place foraging, and sociality.