Barry W. Ache

Olfaction: Diverse Species, Conserved Principles

Olfaction is a vitally important sense for all animals. There are striking similarities between species in the organization of the olfactory pathway, from the nature of the odorant receptor proteins, to perireceptor processes, to the organization of the olfactory CNS, through odor-guided behavior and memory. These common features span a phylogenetically broad array of animals, implying that there is an optimal solution to the problem of detecting and discriminating odors.

Plasma membrane inositol 1,4,5-Trisphosphate-Activated channels mediate signal transduction in lobster olfactory receptor neurons

Inositol 1,4,5-trisphosphate (IP3) selectively evokes an inward (excitatory) current in cultured lobster olfactory receptor neurons (ORNs) and directly activates two types of channels in cell-free patches of plasma membrane from the ORNs. The IP3-activated channels have kinetic properties of odor-activated channels in the ORNs and pharmacological properties of intracellular IP3-activated channels in other systems. An antibody directed against an intracellular, cerebellar IP3 receptor recognizes a protein with a molecular weight similar to the mammalian receptor in the ORNs. The antibody selectively increases odor-evoked inward currents and IP3-activated unitary currents in the ORNs. The data provide further evidence for IP3 as an olfactory second messenger and implicate at least one and possibly two novel plasma membrane IP3 receptors in olfactory transduction.

Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus

SummaryThe aesthetascs of the spiny lobster, Panulirus argus, are hair sensilla located on the lateral filaments of the antennules. Each hair is about 0.8 mm long and innervated by about 320 bipolar sensory neurons, the dendrites of which project as a bundle into the hair shaft. Each of the dendrites develops two cilia. Within a very short distance each of these cilia branches repetitively and dichotomously resulting in 8000 to 10000 outer dendritic segments per hair, or about 20 to 30 branches per neuron. The branches intertwine frequently before running to the tip of the hair. Each hair also possesses inner and outer auxiliary cells. The inner auxiliary cells surround the bundle of dendrites, extending distally to the origin of the ciliary segments. Extensions of these cells project into the bundle of dendrites, separating groups of dendrites into discrete clusters. Outer auxiliary cells wrap the inner ones, but do not extend beyond the base of the hair.

3-Phosphoinositides Modulate Cyclic Nucleotide Signaling in Olfactory Receptor Neurons

Phosphatidylinositol 3-kinase (PI3K)-dependent phosphoinositide signaling has been implicated in diverse cellular systems coupled to receptors for many different ligands, but the extent to which it functions in sensory transduction is yet to be determined. We now report that blocking PI3K activity increases odorant-evoked, cyclic nucleotide-dependent elevation of [Ca(2+)](i) in acutely dissociated rat olfactory receptor neurons and does so in an odorant-specific manner. These findings imply that 3-phosphoinositide signaling acts in vertebrate olfactory transduction to inhibit cyclic nucleotide-dependent excitation of the cells and that the interaction of the two signaling pathways is important in odorant coding, indicating that 3-phosphoinositide signaling can play a role in sensory transduction.

ANTENNULAR CHEMOSENSITIVITY IN THE SPINY LOBSTER, PANULIRUS ARGUS: STUDIES OF TAURINE SENSITIVE RECEPTORS

1. Taurine sensitive receptors in the antennules of the spiny lobster, Panulirus argus, were identified electrophysiologically.2. Recordings from single receptors revealed a narrow and consistent specificity when tested with taurine, taurine analogs and derivatives, and structurally related compounds.3. Taurine was the most stimulatory compound tested. Threshold concentrations for 36 individual receptors ranged from 10-8 to 10-10 M.4. The taurine analogs, hypotaurine and β-alanine, were also very effective but the phosphonic acid analog of taurine was ineffective.5. Regarding receptor specificity, receptor stimulation was greatest with compounds having single terminal basic (amine) and acidic groups separated by two carbon atoms. Compounds having terminal basic and acidic groups separated by three to five carbon atoms were also active. However, activity decreased with the distance of separation of charged groups.6. Alpha-amino acids and compounds with terminal basic and acidic groups separated by only one...

Dual second-messenger pathways in olfactory transduction

Increasing evidence indicates that inositol phosphate as well as cyclic nucleotide signalling pathways mediate olfactory transduction. Both pathways can target multiple ion channel effectors, suggesting that olfactory receptor cells serve as more than simple selectivity filters and that they possibly represent the first stage of olfactory integration.

Processing of antennular input in the brain of the spiny lobster, Panulirus argus

Neurons in the brain of the spiny lobster that respond to chemical and mechanical stimulation of the antennule (antenna I) were recorded and stained intracellularly. Described here are neurons that do not arborize in the olfactory and accessory lobes of the deutocerebrum, but rather primarily target the lateral and/or the median antennular neuropils of the deutocerebrum. Some of the neurons also extend into the antennal and tegumentary neuropils of the tritocerebrum and the neuropils of the median protocerebrum. Included are antennular sensory afferents, antennular motoneurons, projection neurons descending from the central brain, projection neurons ascending from the central brain and projection neurons descending from the eyestalk ganglia. Collectively, these neurons consitutute a novel antennular sensory pathway that is parallel to and independent of the antennular olfactory pathway. The novel pathway integrates mechanosensory and non-olfactory chemosensory information in the lateral and/or the median antennular neuropils, which also serve as lower motor centers of the antennule. Division of the arthropod deutocerebrum into two, functionally distinct chemosensory pathways may reflect differences in how chemosensory information is processed that is fundamental to understanding the origin of the sense of smell.

Immunocytochemical analysis of glomerular regionalization and neuronal diversity in the olfactory deutocerebrum of the spiny lobster.

Abstract.Antibodies against serotonin, dopamine, FMRF amide, substance P, and molluscan small cardioactive peptide (SCPB) were used to differentiate glomeruli and neurons in the olfactory deutocerebrum of the spiny lobster, Panulirus argus. Immunoreactivity to these antibodies identified distinct regions within individual columnar glomeruli of the olfactory lobe (OL), but not within the spherical glomeruli of the accessory lobe (AL). Glomeruli in the lateral, central, and medial layers of the AL, however, had different patterns of immunoreactivity. The immunostainings differentiated six types of local interneurons and three types of centrifugal projection neurons. Local interneurons included: (1) a ”dorsal giant” neuron with serotonin- and FMRF amide-like immunoreactivity arborizing in most or all glomeruli of the OL, in the glomeruli of the medial and lateral layer of the AL and in the unstructured olfactory globular tract neuropil, (2) three large OL ”core” neurons, two with serotonin-like and one with FMRF amide-like immunoreactivity innervating many OL glomeruli, (3) several hundred small, globuli-type OL ”core” neurons with serotonin- and FMRF amide-like immunoreactivity, (4) thousands of small, globuli-type neurons with FMRF amide- and/or substance P-like immunoreactivity connecting the OL with the central layer of the AL, (5) thousands of small, globuli-type AL interneurons with substance P like immunoreactivity and additional arborizations in the unstructured deutocerebral tract neuropil, and (6) many small, globuli-type OL ”rim” neurons with FMRF amide- and/or SCPB-like immunoreactivity. Centrifugal projection neurons included two that targeted the soma clusters and a pair of large neurons with dopamine-like immunoreactivity that originated in the lateral protocerebrum and arborized in the OL and AL glomeruli. Only few ascending projection neurons and no olfactory afferents were labeled. These results suggest that in the spiny lobster neurochemically distinct subpopulations of local interneurons constitute functionally distinct regions within individual OL glomeruli and across groups of AL glomeruli.

Functional organization of olfaction in crustaceans

Abstract Many of the stimulatory components of complex food odors for marine animals such as lobsters and crabs are common, low molecular weight organic molecules. Crustaceans possess very narrowly tuned receptor cells for these substances, which contribute to coding the quality and quantity of food-related odors. Activity evoked by odorant mixtures cannot always be predicted from responses to the individual components of the mixture; this general phenomenon, termed mixture interaction, is a result of events both at the primary receptor cells and in the CNS. With neurons at various levels of the olfactory pathway tractable for physiological, morphological and biochemical analyses, crustaceans provide useful animal models with which to study olfaction.

Voltage- and current-clamp recordings of the receptor potential in olfactory receptor cells in situ

Intracellular recordings obtained using the whole cell configuration of the patch recording technique show that isolated somas of olfactory receptor cells are electrogenic, producing fast overshooting action potentials when depolarized. In situ, these cells produce graded receptor potentials and action potentials when stimulated chemically. The receptor potential can be voltage clamped for analysis of the ionic basis of sensory transduction in olfaction.