A horseradish peroxidase study of the origin of central projections to the rat olfaction bulb

Since its designation in 1896 as a putative olfactory structure, the olfactory tubercle has received little attention in terms of elucidating its role in the processing and perception of odors. Instead, research on the olfactory tubercle has mostly focused on its relationship with the reward system. Here we provide a comprehensive review of research on the olfactory tubercle—with an emphasis on the likely role of this region in olfactory processing and its contributions to perception. Further, we propose several testable hypotheses regarding the likely involvement of the olfactory tubercle in both basic (odor detection, discrimination, parallel processing of olfactory information) and higher-order (social odor processing, hedonics, multi-modal integration) functions. Together, the information within this review highlights an understudied yet potentially critical component in central odor processing.

While portions of the mammalian olfactory system have been studied extensively, the anterior olfactory nucleus (AON) has been relatively ignored. Furthermore, the existing research is dispersed and obscured by many different nomenclatures and approaches. The present review collects and assembles the relatively sparse literature regarding the portion of the brain situated between the olfactory bulb and primary olfactory (piriform) cortex. Included is an overview of the area's organization, the functional, morphological and neurochemical characteristics of its cells and a comprehensive appraisal of its efferent and afferent fiber systems. Available evidence suggests the existence of subdivisions within the AON and demonstrates that the structure influences ongoing activity in many other olfactory areas. We conclude with a discussion of the AON's mysterious but complex role in olfactory information processing.

The organizational patterns of the bilateral projections of the anterior olfactory nucleus (AON) to the main olfactory bulb (MOB) were defined in the rat with Golgi staining, HRP tracing-methods and fluorescent dyes. Three issues were addressed:

• 1.

  (1) description of the morphology of the AON-neurons projecting to the MOB,

• 2.

  (2) quantitative analysis of the bilateral pathways arising in different AON subdivisions and

• 3.

  (3) ultrastructural identification of AON to MOB channels. The cytoarchitectural features of the AON as recognized in Golgi preparations were correlated with its neural architecture as revealed by retrograde HRP-tracing from the MOB. The following cell types were determined:

• 4.

  (1) pyramidal like neurons typified by a lack of basal dendrites and a sparse covering with long spines (pars externa),

• 5.

  (2) fusiform shaped cells with bipolar dendritic arborisations (pars medialis) and

• 6.

  (3) densely spined fusiform, pyramidal and polygonal neurons (pars ventroposterior, lateralis and dorsalis) with a tendency of radial orientation of their apical dendrites. In addition, in the more caudal parts of the pars ventroposterior there were neurons with tertiary dendritic processes oriented nearly parallel to the molecular layer. Quantitative analysis of AON neurons projecting to the MOB showed that the pars externa neurons project exclusively to the contralateral MOB while pars medialis neurons project almost exclusively to the ipsilateral MOB. All subdivisions of the AON which establish specific termination patterns within the MOB, participated in about equal portion in the ipsilateral projections to the MOB. The highest proportion of the bilaterally projecting neurons were found in the dorsal subdivision, followed by the lateral and ventroposterior subdivisions. The postsynaptic targets of the AON to MOB channel are the spinous processes and varicosities of the proximal and distal-most dendrites of granule cells. The boutons derived from AON projection neurons contained clear spherical vesicles and established exclusively asymmetric synaptic junctions.

Immunocytochemical localization of specific neurotransmitters in the brain is becoming increasingly important in studies of maturation. We have used the trilaminar prepyriform cortex (PC) of rats to study the distribution, patterns and relative number of cells, fibers and terminals during postnatal development using antisera to cholecystokinin (CCK) and glutamic acid decarboxylase (GAD). Both antisera show distinct patterns of immunoreactivity at birth and subsequent periods of distinct changes in these patterns. CCK immunoreactivity is rare but present at birth mostly in layer II. There is a dramatic increase of CCK-labeled structures between postnatal (PN) days 6 and 9 and between PN 13 and 21. The adult pattern is observed by PN 21 with large numbers of labeled cells in layer II, numerous terminals in layers II and deep I and large immunoreactive fibers in the lateral olfactory tract. At birth GAD-immunoreactive terminals are present mainly in layer I, forming a distinct pattern of superficial and deep bands. Subsequent major changes occur in this pattern between PN 9 and 13 and again between PN 13 and 21. By PN 21 there appears to be a loss in deeper laminae of GAD positive terminals which are possibly replaced by the increasing numbers of CCK terminals in the same sublaminae. The adult pattern of GAD immunoreactivity is established by PN 21 with terminals and a few cells in layer I. Therefore, throughout development of the rat PC, there is a distinct complementary and changing distribution of GAD and CCK. Factors that may influence these changes in immunoreactivity are discussed.

Neuronal activities following olfactory bulb electrical stimulation were examined before and after administration of dopamine and dopamine antagonist in the rat olfactory tubercle. The inhibitory response to olfactory bulb stimulation was attenuated by systemic haloperidol administration, but the excitatory response to olfactory bulb stimulation rarely was modulated. Topical application of dopamine by iontophoresis extended the duration of inhibition in 56% of the neurons sampled and diminished it in 25%; the excitatory response was modulated in 42% of neurons, most of which were attenuated. These findings suggest that dopamine in the olfactory tubercle could be involved in modulations of neuronal activities related to olfactory transduction.