Unilateral lesions of the olfactory tubercle modifying general arousal effects in the rat olfactory bulb

doi:10.1016/0013-4694(79)90104-4

Electroencephalography and Clinical Neurophysiology

Volume 46, Issue 6, June 1979, Pages 665-674

https://doi.org/10.1016/0013-4694(79)90104-4 Get rights and content

Abstract

The centrifugal control exerted by different arousal states on the rat olfactory bulb was investigated. The olfactory tubercle was unilaterally coagulated with either 1 mA or 3 mA current. The vigilance state parameters and multiunit mitral cell activity were recorded in freely moving rats, stimulated either by their usual food odor or by isoamyl acetate, in a hungary or a satiated state. In each animal, a unilateral lesion affected resting activity and the relative proportion of positive (excitatory) and negative (inhibitory) responses in the same way in both olfactory bulbs; these effects were proportional to the extent of the lesion. In wakefulness, a nutritional modulation of the bulb responses for food odor existed in spite of a slight decrease in the general arousal level. In slow wave sleep (SWS), when compared to a control group, the rats with lesions showed an increase of neocortical desynchronization induced by olfactory stimulation, and a large decrease of mitral cell excitability. Inhibition of the olfactory input, which normally develops during SWS, could involve mainly mesencephalic neurons reaching the olfactory tubercle and the bulb via the ventral part of the medial forebrain bundle.

Résumé

On a étudié chez le rat, le contrôle centrifuge de l'activité du bulbe olfactif au cours des divers états de vigilance. Le tubercule olfactif a été électrocoagulé unilatéralement avec des intensités de courant de 1 ou 3 mA. Les paramètres permettant de déterminer l'état de vigilance et l'activité multiunitaire des cellules mitrales ont été enregistrés en conditions chroniques, chez les rats affamés ou rassasiés, et stimulés par l'odeur de leur aliment habituel ou l'acétate d'isoamyle. Chez chaque sujet les lésions unilatérales ont modifié l'activité de repos et les proportions de réponses par excitation et par inhibition d'une façon identique dans les deux bulbes olfactifs; ces modifications étaient proportionnelles à l'étendue de la lésion. Lors de l'éveil, la modulation des résponses bulbaires à l'odeur alimentaire était effective en dépit d'une faible diminution du tonus activateur de l'éveil général. Lors du sommeil lent (SL), les lésions ont entraîne, relativement à un groupe contrôle, une augmentation de la proportion des désynchronisations néocorticales induites par les stimulations, en même temps qu'une chute de l'excitabilité des cellules mitrales. L'inhibition de l'entrée olfactive qui se développe normalement au cours du SL, impliquerait principalement l'action de neurones d'origine mésencéphalique qui se projettent sur le tubercule et le bulbe olfactif par le faisceau télencéphalique médian ventral.

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The olfactory tubercle (OT), an important nucleus in processing sensory information, has been reported to change cortical activity under odor. However, little is known about the physiological role and mechanism of the OT in sleep-wake regulation. The OT expresses abundant adenosine A_2A receptors (A_2ARs), which are important in sleep regulation. Therefore, we hypothesized that the OT regulates sleep via A_2ARs. This study examined sleep-wake profiles through electroencephalography and electromyography recordings with pharmacological and chemogenetic manipulations in freely moving rodents. Compared with their controls, activation of OT A_2ARs pharmacologically and OT A_2AR neurons via chemogenetics increased non-rapid eye movement sleep for 5 and 3 h, respectively, while blockade of A_2ARs decreased non-rapid eye movement sleep. Tracing and electrophysiological studies showed OT A_2AR neurons projected to the ventral pallidum and lateral hypothalamus, forming inhibitory innervations. Together, these findings indicate that A_2ARs in the OT play an important role in sleep regulation.
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Unilateral OTu lesions affect the spontaneous and odor-evoked activity of OB mitral cells, suggesting that OTu may be involved in modulation of OB odor responses. Further, unilateral lesion of the OTu increases neocortical desynchronization (arousal) induced by olfactory stimulation during slow wave sleep, suggesting a modulation of olfactory-mediated cortical arousal by the OTu (Gervais, 1979). Taking into account the FAA-associated oscillation of the OTu׳s metabolic activity, the OTu may also contribute to FAA by modulating the arousal state of rabbit pups through an integration of olfactory signals with cortical regions that are part of behavioral arousal control.
Animals maintained under conditions of food-availability restricted to a specific period of the day show molecular and physiological circadian rhythms and increase their locomotor activity 2–3 h prior to the next scheduled feeding, called food anticipatory activity (FAA). Although the anatomical substrates and underlying mechanisms of the food-entrainable oscillator are not well understood, experimental evidence indicates that it involves multiple structures and systems. Using rabbit pups entrained to circadian nursing as a natural model of food restriction, we hypothesized that the anterior piriform cortex (APCx) and the olfactory tubercle (OTu) are activated during nursing-associated FAA. Two groups of litters were entrained to one of two different nursing times. At postnatal day 7, when litters showed clear FAA, pups from each litter were euthanized at nursing time, or 1, 2, 4, 8, 12, 16 or 20 h later. Neural metabolic activities of the APCx, OTu, olfactory bulb (OB) and suprachiasmatic nucleus (SCN) were assessed by cytochrome oxidase histochemistry. Additionally, two fasted groups were nurse-deprived for two cycles before being euthanized at postnatal day 9. In nursed pups, metabolic activity of APCx, OTu and OB increased during FAA and after feeding, independently of the geographical time. Metabolic activity in SCN was not affected by nursing schedule. Given that APCx and OTu are in a key network position to integrate temporal odor signals with body energetic state, brain arousal and reward mechanisms, we suggest that these structures could be an important part of the conditioned oscillatory mechanism that leads to food entrainment.
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The olfactory tubercle, along with the piriform cortex, is highly activated during tasks engaging attention (Zelano et al., 2005). This finding is in parallel to the earlier rodent work linking the olfactory tubercle to arousal-related systems (see Gervais, 1979; Ikemoto, 2007). Additional work from the same group (Zelano et al., 2007) suggests that the olfactory tubercle may be crucial in sorting out the source of olfactory information (trigeminal stimulants vs. pure olfactory).
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A very regular 8–12 rhythm was found in the olfactory tubercle of the armadillo Chaetophractus villosus. The rhythm was observed during wakefulness. Considerable sinusoidal activity was also observed not only during wakefulness, but during synchronized (slow) and desynchronized (paradoxical) sleep. The significance of this novel rhythm is discussed together with considerations at establish an important difference between it and the other ‘alpha rhythms’ known.
Un rythme de 8 à 12 très régulier a été trouvé dans le tubercule olfactif du tatou Chaetophractus villosus. Le rythme a été observé au cours de l'éveil. Une nette activité sinusoïdale a également été observée, non seulement pendant l'éveil, mais aussi pendant le sommeil avec tracé synchronisé (lent) ou désynchronisé (paradoxal). La signification de ce nouveau rythme est discutée; on souligne la différence importante entre ce rythme et les autres ‘rythmes alpha’ connus.
Effect of local 5,6-dihydroxytryptamine on the rat olfactory bulb responsiveness during wakefulness and sleep
1984, Electroencephalography and Clinical Neurophysiology
This study investigated a possible participation of the centrifugal serotonergic (5-HT) innervation of the olfactory bulb (OB) in the control of the multiunit mitral cell responsiveness in behaving rats. A bilateral injection of 5,6-dihydroxytryptamine solution (5,6-DHT) into the OB induced in this structure an average 70% reduction in the level of endogenous serotonin. Control and treated animals were habituated to eat a single 2 h daily meal. Recording sessions were performed either after a 22 h fasting period or just after the meal. The summated multiunit mitral cell activity and vigilance state parameters were recorded in the absence of and during repeated stimulation by puffs of food odour and isoamyl acetate. The results showed that the 5,6-DHT treatment did not modify significantly previously established centrifugal controls exerted at the OB level: (1) the selective enhancement of the mitral cell responsiveness to food odour occurring in waking food-deprived animals; (2) the inhibition of the olfactory input during slow wave sleep. However, the considered 5-HT projections could mediate some inhibitory influence on mitral cell activity during wakefulness only. Finally, the 5-HT innervation of the OB did not seem to be involved in basic mechanisms of olfactory recognition.
Ce travail étudie le rôle de l'innervation sérotoninergique (5-HT) du bulbe olfactif (BO) dans le contrôle de la réactivité multiunitaire des cellules mitrales chez le rat non contraint. L'injection intrabulbaire bilatérale d'une solution de 5,6-dihydroxytryptamine (5,6-DHT) entraîne une réduction moyenne de 70% de la concentration de sérotonine bulbaire. Les animaux témoins et traités sont habitués à consommer un unique repas quotidien de 2 h. Les séances d'enregistrement ont été réalisées, soit après une période de 22 h de jeûne, soit juste après le repas quotidien. L'activité multiunitaire intégrée des cellules mitrales et des paramètres servant à objectiver les états de vigilance ont été enregistrées en l'absence et pendant la présentation itérative de bouffées d'odeur alimentaire et d'acétate d'isoamyle. Les résultats montrent que le traitement par la 5,6-DHT ne modifie pas significativement l'expression des contrôles centrifuges qui s'exercent normalement à l'étage bulbaire et qui sont responsables de: (1) l'augmentation sélective de la réactivité bulbaire à l'odeur d'aliment qui se manifeste pendant la veille chez l'animal en état de faim; (2) la faible sensibilité de l'appareil olfactif aux odeurs lors du sommeil à ondes lentes. Les projections 5-HT étudiées pourraient toutefois exercer pendant la veille un effet inhibiteur sur l'activité des cellules mitrales. Enfin, l'innervation 5-HT du BO ne semble pas nécessaire aux processus de discrimination olfactive.

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¹: Doctoral scholarship from the French Government.

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Unilateral lesions of the olfactory tubercle modifying general arousal effects in the rat olfactory bulbModifications de quelques effets des états de vigilance induites au niveau du bulbe olfactif par la lésion unilatérale du tubercule olfactif chez le rat

Abstract

Résumé

Physiol. Behav.

Brain Res.

Brain Res.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Brain Res.

Brain Res.

Brain Res.

Exp. Neurol.

Physiol. Behav.

Physiol. Behav.

Brain Res.

Exp. Neurol.

Hypothalamic influences on the electrical activity of the olfactory pathway

Brain Res. Bull.