The physiology of olfaction in insects.
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Olfactory research is entering a new phase, in which molecular mechanisms are being revealed that go considerably beyond traditional concepts. New ways of characterizing these mechanisms are needed, and some suggestions toward that goal have been made in this review. These suggestions recognize that, whereas formerly our terms and concepts regarding olfactory stimulus-response characteristics came mainly from organic chemists and psychophysicists, the main impetus at present comes from molecular biology. A desirable terminology, therefore, is one that is familiar to molecular biologists and can facilitate comparisons with other systems--immune, endocrine, nervous--where similar methods and terms are in use. The suggestions made here for the olfactory system could also be adapted for the taste system. Taste stimulation could be characterized, for example, in terms of gustagens interacting with G-cell receptors, stimulation being determined by the gustatope of a particular ion or molecule. It should be emphasized that such terms and mechanisms may not need to be invoked in studies at behavioral or psychophysical levels. However, the need for them at the receptor level may well be an accurate reflection of our progress in applying methods of molecular biology to these systems.
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We have investigated the roles of the putative cyclic nucleotide-modulated K+ channel subunit encoded by the ether a go-go (eag) gene and a voltage-gated Na+ channel, smellblind (sbl), encoded by the paralytic (para) locus in odorant responsiveness and cell excitability in Drosophila melanogaster. Three independent mutant alleles of eag revealed reduced antennal responsiveness in adult flies to a subset of odorants, all having short aliphatic side chains: ethyl butyrate (EB), propionic acid, 2-butanone and ethyl acetate (manuscript submitted). Loose patch recordings revealed that significantly fewer eag antennal neurons responded to EB compared to control neurons. As expected if Eag were involved in odor transduction, fewer EB-induced inhibitory responses were observed in eag mutants and focal application of high K+ saline to sensillae altered the excitability of the majority of neurons from wild-type, but not eag, antennae. Interestingly, there were fewer excitatory odorant responses dependent on extracellular Ca2+ in eag neurons. In contrast to the involvement of Eag in adult olfactory neuron odorant transduction, we found no evidence that adult sbl and allelic olfactory D (olfD) gene mutants were defective in their behavioral response to a complex attractive odor. Furthermore, electrophysiological analyses of adult sbl and olfD mutants revealed normal electroantennogram responses to a broad range of individual pure odorants and no changes in the excitable properties of olfactory neurons as determined by loose patch recordings.
To investigate the neural encoding of glutamate (umami) taste in the primate, recordings were made from taste responsive neurons in the cortical taste areas in macaques. Most of the neurons were in the orbitofrontal cortex (secondary) taste area. First, it was shown that there is a representation of the taste of glutamate which is separate from the representation of the other prototypical tastants sweet (glucose), salt (NaCl), bitter (quinine) and sour (HCl). Second, it was shown that single neurons that had their best responses to sodium glutamate also had good responses to glutamic acid. Third, it was shown that the responses of these neurons to the nucleotide umami tastant inosine 5'-monophosphate were more correlated with their responses to monosodium glutamate than to any prototypical tastant. Fourth, concentration response curves showed that concentrations of monosodium glutamate as low as 0.001 M were just above threshold for some of these neurons. Fifth, some neurons in the orbitofrontal region, which responded to monosodium glutamate and other food tastes, decreased their responses after feeding with monosodium glutamate to behavioral satiety, revealing a mechanism of satiety. In some cases this reduction was sensory-specific. Sixth, it was shown in psychophysical experiments in humans that the flavor of umami is strongest with a combination of corresponding taste and olfactory stimuli (e.g., monosodium glutamate and garlic odor). The hypothesis is proposed that part of the way in which glutamate works as a flavor enhancer is by acting in combination with corresponding food odors. The appropriate associations between the odor and the glutamate taste may be learned at least in part by olfactory to taste association learning in the primate orbitofrontal cortex.
In a series of studies we have been exploring the role of hippocampal function in memory using the model system of olfactory-hippocampal pathways and odor learning in rats. Our experiments show that hippocampus itself is not essential to memory for single odors, but is critical for forming the representations of relations among odor memories, and for the expression of odor memory representations in novel situations. These studies that exploit the exceptional qualities of olfactory learning are helping to clarify the nature of higher order memory processes in all mammals, and extending to declarative memory in humans.
Positron emission tomographic (PET) scanning can be used to assess the cortical processing of responses to different odorants in man. The olfactory bulb receives the first projections on an ipsilateral basis from the nose, but then the cortex and the limbic system respond bilaterally. More irritating, burning odors (e.g., acetone) project via the trigeminal rather than the olfactory nerve and induce changes in the brain stem and the cortex. Sweet and salty tastes are readily distinguishable, but a bitter or painful stimulus leads to a deactivation of the primary gustatory cortex, which is in keeping with the need to focus on an avoidance response. The complex discrimination of odors, however, seems to involve the insula cortex, cerebellum, and hypothalamus, with pheromones seemingly sensed via the olfactory system in humans.
Samples of 12 hospitalized Korsakoffs, 12 hospitalized non-Korsakoff alcoholics, and 12 controls, all groups being of comparable age range, were tested using a set of seven visual and olfactory measures which involved memory. By stepwise multiple discriminant analysis it was shown that strong separation could be effected between the three groups, solely on the basis of the olfactory recognition and recall tests, which included the Campbell-Gregson (1972) procedure. The use of of anosmia as a diagnostic indicator for Korsakoff's syndrome is discussed.
Olfactory perception and related emotions are largely dependent on inspiration. We acquired simultaneous respiration and electroencephalographic recordings during pleasant odour and unpleasant odour stimulation. We sought to identify changes in respiratory pattern, inspiratory-related potentials and location of dipoles estimated from the potentials. Electroencephalographic recording was triggered by inspiration onset. Respiratory frequency decreased at pleasant odour recognition, and it increased at unpleasant odour detection and recognition. O2 consumption records showed that these changes were not due to metabolic demand. During olfactory stimulation, inspiratory phase-locked alpha oscillation (I-alpha) was found in the averaged potential triggered by inspiration onset. I-alpha was observed at both pleasant odour and unpleasant odour detection and recognition, but it was not seen in the inspiration-triggered potentials of normal air breathing. Electroencephalographic dipole tracing identified the location of dipoles from the I-alpha in the limbic area and the cortex; the entorhinal cortex, hippocampus, amygdala, premotor area and centroposterior orbitofrontal cortex subserve odour detection, and the rostromedial orbitofrontal cortex subserves odour recognition. We suggest that the I-alpha in our study originated from the olfactory cortex in the forebrain and was phase-locked to inspiration.
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