Though the olfactory bulb extends well in front of the forebrain along a stalk known as the olfactory tract, it is derived from the ventral pallium during development and is part of the telencephalon. The olfactory bulb is divided into two regions: the main olfactory bulb anteriorly and the accessory olfactory bulb posteriorly. The olfactory bulb generally consists of six architectonic layers. From dorsal to ventral they are the layer of the olfactory nerve fibres, the glomerular layer, the outer plexiform layer, the mitral layer, the inner plexiform layer, and the granular layer (75). A second granular layer, called the external granular layer, may be present below the glomerular layer. It is often absent or indistinguishable from the glomerular layer. However, one study found no laminar organization in the main olfactory bulb and only two layers to the accessory
olfactory bulb: a dorsal plexiform layer and a ventral cellular layer, suggesting that cytoarchitectural organization in this nucleus may vary by species (85).
In the mammalian literature, the olfactory bulbs together with the olfactory peduncle are traditionally referred to as the rhinencephalon. We have never encountered this term in the squamate neurobiological literature and will avoid using it here.
2.2.1 Main Olfactory Bulb
Cellular Neurochemistry
The inner granular and internal plexiform layers contain light-staining aromatase expressing cells, while the mitral and external plexiform layers contain dark-staining aromatase expressing cells (39). Dopamine receptors are expressed by cells in the mitral layer, and to a lesser extent in the external plexiform, glomerular, and internal plexiform layers, while tyrosine hydroxylase is mainly expressed in the glomerular layer (53). A few cells expressing nitric oxide are scattered around the periphery of the olfactory bulb (97). The olfactory bulb shows the highest aromatase activity anywhere in the squamate brain and conversion of testosterone to estrogen is greater in the spring compared to the fall (123). Tbr-1 and doublecortin are expressed, but not co-expressed in the same neuronal cell bodies (79).
Connectivity and Fibrous Neurochemistry
The main olfactory bulb receives its principle projections from the olfactory sensory neurons of the nostril and it is the first relay for all olfactory information entering the brain (124). In addition, the retrobulbar formation, diagonal band of Broca and the ventral lateral cortex send projections back to the main olfactory bulb (119). Cholinergic projections to the olfactory bulb originate from the nucleus of the diagonal band and the substantia innominata (102). Fibres co-expressing tyrosine hydroxylase and neuropeptide-FF are found in the internal granular layer (53, 96). Scattered orexinergic and thyrotropin-releasing hormone terminals also project to the internal granular (54, 125). In contrast, fibres expressing gonadotropic-releasing hormone are diffused through all layers except the internal granular layer (22).
The olfactory bulb sends massive bilateral projections to the superficial plexiform layer of the lateral cortex, and additionally projects to the anterior olfactory nucleus, external and ventral anterior amygdalar nuclei, olfactory tubercle, and the diagonal band of Broca (102).
Neurogenesis
The olfactory bulb is the site of perhaps the most intense recruitment of neurons some species of squamates, though in others recruitment is stronger in the medial cortex (29, 73, 75, 78). Neurogenesis does not occur in the olfactory bulb (73). Instead, neurons are generated along the ependymal layer of the lateral ventricle in the rostral forebrain (126). They then undergo the only long-distance migration of neurons known in vertebrates (73). These neurons travel along a highly restricted migratory route known as the rostral migratory stream from the rostral forebrain through the olfactory tract to the olfactory bulb (73, 126). There, they are integrated mostly into the granular cell layer (73, 75). Some new neurons are integrated into the mitral and glomerular layers (75). Neurogenesis in the ependymal layer of the lateral ventricle is greater in the spring and summer compared to the fall and winter (82, 83). Transport along the restricted migratory route slows in the summer and neurons reach the olfactory bulb primarily in the other three seasons (78). Males seem to have a higher rate of neuronal recruitment, mirroring the lateral cortex to which the main olfactory bulb has its most significant projections (122).
2.2.2 Accessory Olfactory Bulb
Cytoarchitecture and Cellular Neurochemistry
Rostrally, the accessory olfactory bulb usually consists of the six layers of the olfactory bulb, however caudally only three layers remain: the external plexiform, mitral, and internal granular layers (39, 75). Aromatase is expressed prominently in the external plexiform and mitral layers, and less prominently in the internal granular layer (39). Dopamine receptors are expressed mostly by cells in the mitral layer, but are also found in the external plexiform, glomerular, and internal plexiform layers, while tyrosine hydroxylase is expressed by the glomerular layer (53). Some neurons also express nitric
oxide synthase (127). As in the main olfactory bulb, Tbr-1 and doublecortin are expressed, but not co-expressed in the same neuronal cell bodies (79).
Connectivity and Fibrous Neurochemistry
The accessory olfactory bulb receives projections from vomeronasal chemoreceptor neurons in the vomeronasal organ (Jackobson’s organ) and the tongue (124). Its primary projections are to the hilus of the ipsilateral spherical nucleus (119). It also projects to the medial and accessory olfactory amygdaloid nuclei as well as to the olfactory tubercle (119) 1997). Although the accessory olfactory bulb projects ipsilaterally to the spherical nucleus, reciprocal projections from the spherical nucleus to the accessory olfactory nucleus are bilateral (119). They terminate bilaterally on the granular layer and ipsilaterally on the internal plexiform layer (119). The accessory olfactory bulb also receives projections from the bed nucleus of the terminal groove (102, 128). Fibres expressing tyrosine hydroxylase and neuropeptide-FF project to the internal granular layer and fibres expressing gonadotropin releasing hormone project to all layers except the internal granular layer (22, 53, 96).
Functional Correlations
The accessory olfactory bulb is the first recipient of vomeronasal information from the tongue and vomeronasal organ (129). These detect chemicals that have a higher molecular weight than the olfactory system, including pheromones. As such, the accessory olfactory bulb likely plays a role in reproduction, as it does in other vertebrates (1). The accessory olfactory bulb is sexually dimorphic, being larger in males than females (122).
Neurogenesis
The accessory olfactory bulb recruits neurons in the same way as the main olfactory bulb (section 2.2.1). Neurons travel from the proliferation zone of the lateral ventricles along the olfactory peduncle and are deposited primarily in the granular layer (126).
2.2.3 Anterior Olfactory Nucleus
The anterior olfactory nucleus is situated at the base of the olfactory tract in the rostral telencephalon in a region referred to as the retrobulbar formation. Anterior olfactory neurons express androgen receptors, dopamine receptors, nitric oxide, Tbr-1 and neuropeptide-FF (53, 79, 96, 130). It receives ipsilateral projections from the main olfactory bulb and bilateral projections from the lateral cortex, and projects back to the lateral cortex as well as the to dorsal cortex (50). Projections to the anterior olfactory nucleus express dopamine receptors, calcitonin gene-related peptide and neuropeptide- FF (53, 96).
The anterior olfactory nucleus sits at the rostral extent of the lateral ventricles and is the site of neurogenesis for the neurons that will be transported to the olfactory bulb (78). As with elsewhere along the lateral ventricle, new neurons are generated from radial glial cells in the ependymal layer and then migrate to their destinations (82). Proliferation varies by season and peaks in the spring and summer (82). New neurons are also incorporated into the cell layer of the anterior olfactory nucleus (73, 78).