The functional organization of the fish olfactory system

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Abstract

Recent developments in the functional anatomy and physiology of the fish olfactory system reveal three parallel pathways from the sensory epithelium, via the olfactory bulb to the telencephalon. There are three morphological types of sensory neurones spread in a seemingly overlapping arrangement in the olfactory epithelium. The axons of each type of sensory neurones converge to a specific region of the olfactory bulb and connect to separate sets of relay neurones. The axons of these relay neurones leave in three bundles to the telencephalon. Each bundle conveys specific information that elicits sets of characteristic behaviour in response to odours involved in essential life processes in the fish. One pathway is tuned to social cues, another to sex pheromones, and the third to food odours.

Section snippets

Odorants of essential life processes

It is commonly acknowledged that life is dependent upon three fundamental processes, viz. reproduction, feeding and avoidance. In fishes, these functions can be mediated via the olfactory system and by different classes of molecules, i.e., amino acids, bile salts, pheromones. Yet, the odorants are mixed in their natural environment. How can fish distinguish between these complex odorants, and how do the fish know what is the appropriate behaviour pattern at the different seasons? In other

Anatomy

The layout of the olfactory system is demonstrated in the photo of the exposed brain of the crucian carp (Fig. 1). As in all vertebrates the primary sensory neurones are located in the sensory epithelium, which in fishes is called the olfactory rosette, because the leaf-like structures of the lamellae resemble a miniature rose. The sensory neurones have thin axons that terminate in the olfactory bulb in specific synaptic structures called glomeruli. In these aggregates of terminals many

Sensory neurones

The sensory neurones that make up the assembly of cells detecting the odorants in fishes constitute three types with different shapes. These are the ciliated sensory neurones, with long dendrites and a few cilia; the microvillous sensory neurones with shorter dendrites than the ciliated cells and have microvillae extending from their apical surface (Thommesen, 1983, Yamamoto and Ueda, 1979). The third cell type is called crypt cells (Hansen et al., 1997, Hansen and Finger, 2000). These latter

Behaviour and tract bundles

The understanding of the chemotopic representation of odour information in fish was initiated when it was shown that electric stimulation of a particular bundle of the olfactory tract evoked distinct behaviours in free swimming cods (Døving and Selset, 1980). The tracts bundles have been given anatomical names due to their anatomical position, viz., medial (MOT) and lateral (LOT) olfactory tract, and each bundle has a medial and lateral portion. Stimulation of the medial part of the medial

Pathways within the olfactory system

What is the relation between the olfactory sensory neurones and the different tract bundles? The existence of three bundles within each olfactory tract and three morphological different sensory neurones could be a simple coincidence but it could also reflect a functional distinction. We sought the answer to this question by discrete application of DiI crystals to the glomerular region of the olfactory bulb. If properly applied, the stain will diffuse from this synaptic region both along the

Specificity of the different types of sensory neurones

Thommesen (1983) correlated the amplitudes of the EOG (electro-olfactogram) responses to amino acids and bile salts with the relative densities of sensory neurones in the sensory epithelium of salmonids. The ciliated sensory neurones were more abundant in the peripheral part of the olfactory rosette than in the central part, while the microvillous sensory neurones were more abundant in the central part than in the peripheral region. The amplitudes of EOG responses were larger to amino acids

The molecular entities in the olfactory receptor neurones

Each sensory neurone expresses only one particular odorant receptor and seems randomly distributed within the sensory epithelium. Yet, they send the axons to the olfactory bulb in an organized manner that yields a stereotyped map. Because the sensory neurones differ in morphology and their bulbar projections, it is reasonable to suppose that they differ in the expression of the G-proteins and odorant receptor molecules. This notion has been confirmed in a number of studies, revealing a

Responses of bulbar neurones to odorants

The correlation between the different ORN phenotypes and their axon projections into discrete neuropils called glomeruli make the basis for a chemospecific map in the olfactory bulb. Thus, within the bulb each class of odorants is represented by a distinct glomerular zone; in contrast to what is found in the olfactory epithelium. The glomerulus is a centre for integration of the olfactory information captured by a specific odorant receptor located on coarsely distributed ORNs.

In general, the

Labelled lines within labelled lines

The reproductive behaviour is mediated by the lateral part of the medial olfactory tract, and this part of the olfactory tract leaves the bulb in the ventral region. It was in the ventral region that Friedrich and Korsching (1998) found glomeruli responding to sex pheromones and the crypt cells which express Gαo or Gαq proteins project to the ventral region of the olfactory bulb in catfish (Hansen et al., 2004). We have shown that neurones in this part of the bulb respond specifically to sex

Conclusions and perspectives

The studies reviewed here illustrate a remarkable division of the teleost olfactory system. There are three morphological types of sensory neurones, each type equipped with specialized receptors and G-proteins, suggesting distinct transduction mechanisms. These sensory neurones are spread over the sensory epithelium seemingly at random, but the axons of each type of sensory neurones project to discrete regions of the olfactory bulb where they make synapses with the relay neurones.

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