The importance of central noradrenergic influences on the olfactory bulb in the processing of learned olfactory cues

Gervais, R.; Holley, André Ah; Keverne, Barry

doi:10.1093/chemse/13.1.3

Cited by 67 publications

(27 citation statements)

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“…An increase in noradrenaline in response to muscimol challenges has also been reported in the sheep main olfactory bulb [14] and is probably due to the action of the GABA A receptor agonist on the noradrenergic presynaptic terminals [4]. Therefore, such local control of noradrenaline release by activation of GABA A receptors is probably important for enhancing the release of noradrenaline in the vicinity of the AOB mitral cells responding to male pheromones and thereby leading to the formation of the pheromone-specific memory as previously suggested [5]. This hypothesis is supported by the finding that bicuculline-induced memory lacks the pheromone specificity of the memory formed at mating and appears to generalize to the pheromones of at least one other strain [11].…”

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confidence: 64%

Activation of GABAA Receptors in the Accessory Olfactory Bulb Does Not Prevent the Formation of an Olfactory Memory in Mice.

Otsuka

Hashida

Oka

et al. 2001

The Journal of Veterinary Medical Science

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ABSTRACT. When female mice are mated, they form a memory to the pheromonal signal of their male partner. The neural mechanisms underlying this memory involve changes at the reciprocal dendrodendritic synapses between glutamatergic mitral cells and γ-aminobutyric acid (GABA)-ergic granule cells in the accessory olfactory bulb (AOB). Blockade of GABA A receptors in the AOB leads to the formation of an olfactory memory. In an attempt to disrupt memory formation at mating, we used local infusions of the GABA A receptor agonist muscimol into the AOB during the critical period for memory formation. Muscimol across a wide range of doses (1-1000 pmol) did not prevent memory formation. The resistance of this memory to GABA A receptor activation may reflect the complexity of synaptic microcircuits in the AOB. KEY WORDS: accessory olfactory bulb, GABA A receptor, olfactory memory.J. Vet. Med. Sci. 63 (7): [807][808][809] 2001 The reproductive physiology of mammals is strongly influenced by pheromones, with some of the most dramatic effects elicited in mice. Urinary male pheromones activate the vomeronasal system, by way of the vomeronasal receptors, and promote mating by inducing estrus in female mice [12]. However, if this pheromonal effect is induced within three days after mating, implantation of the embryos is prevented. This is referred to as the olfactory block to pregnancy and often occurs if a recently mated female is exposed to the pheromones of an unfamiliar male. To prevent the male partner from blocking pregnancy of his mate, the female forms a memory for the pheromones of her male partner. Several features which characterize the neural basis of this olfactory recognition memory have now been elucidated [1,2,8]. Memory formation depends on vaginocervical stimulation at mating [13], but requires a prolonged exposure of 4-6 hr to male pheromones immediately after mating [18]. The formation, but not recall, of the memory depends on mating-induced enhancement of α-adrenergic transmission in the accessory olfactory bulb (AOB), the first relay in the vomeronasal system [7,13,18]. This memory lasts for at least 30 days following mating unless pregnancy ensues [11]. The neural changes underlying the long-lasting memory occur in the AOB [11].Microcircuits in the AOB include the prominent reciprocal dendrodendritic synapse between mitral and granule cells. Glutamate released from mitral cell dendrites activates the dendrites of granule cells, which in turn mediate γ-aminobutyric acid (GABA)-ergic dendrodendritic inhibition back onto mitral cell dendrites [6]. This feedback inhibition at the reciprocal synapses regulates mitral cell activity [7,15]. The formation of the pheromonal memory involves changes at the reciprocal synapses [3,16]. The GABAmediated feedback inhibition through the granule-to-mitral synapse is very powerful and is the main means for mediating control of output from the AOB, activating neuroendocrine mechanisms via the hypothalamus [7,10,15]. Blockade of GABA A receptors by local infusions of bicuc...

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supporting

confidence: 64%

Activation of GABAA Receptors in the Accessory Olfactory Bulb Does Not Prevent the Formation of an Olfactory Memory in Mice.

Otsuka

Hashida

Oka

et al. 2001

The Journal of Veterinary Medical Science

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“…Evidence-in particular, that of Walter Freeman and his coworkers-indicates that, with repeated reinforced exposure, odor-specific bursts of neural activity are produced from the surface of the olfactory bulb (see, e.g., Carmi & Leon, 1991;Chaput & Holley, 1985;Coop-ersmith & Leon, 1984;Freeman & Grajski, 1987;Grajski & Freeman, 1986, 1989Sullivan, Wilson, & Leon, 1989). Furthermore, learning has been shown to produce odorrelated synaptic changes in both the bulb (Gervais, Holley, & Keverne, 1988;Grajski & Freeman, 1989;Gray, Freeman, & Skinner, 1986;Nicoll & Jahr, 1982;Sullivan et aI., 1989;Wilson & Sullivan, 1991) and olfactory cortex (Haberly & Bower, 1989;Kauer, 1987;Schild, 1988). It is possible, therefore, that, through learning and association, these changes are the basis on which object odors come to be recognized as single entities.…”

Section: Discussionmentioning

confidence: 99%

The influence of chemical complexity on the perception of multicomponent odor mixtures

Livermore

Laing

1998

Perception & Psychophysics

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The present study investigates the hypothesis that complex object odors (odors that emanate from flowers, foods, sewage, etc.) that consist of dozens of odorants are processed and encoded as discrete entities, as if each was a single chemical odor. To test this hypothesis, the capacity of trained subjects to discriminate and identify the components of stimuli consisting of one to eight object odors was determined. The results indicated that subjects could only identify up to four object odors in a mixture, which is similar to earlier findings with mixtures that contained only single chemical odors. The limited capacity was also reflected in the number of odors selected, regardless of whether the choices were correct or incorrect, in confidence ratings, and in decision times. The identification of a limited number of object odors in every mixture that was presented suggests that both associative (synthetic) and dissociative (analytic) processes are involved in the perceptual analysis of odor mixtures.

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“…In mammalian olfactory systems the necessity of modulatory input from outside the olfactory bulb for behavioral modification of olfactory bulb electrophysiology is well documented (Gervais et al 1988;Gray et al 1986). We have shown that the coherent network oscillation in LFP displayed by the PC is modulated in frequency and waveform by dopamine and serotonin .…”

Section: Discussionmentioning

confidence: 99%

Cultured olfactory interneurons from Limax maximus: optical and electrophysiological studies of transmitter-evoked responses

Rhines

Sokolove

Flores

et al. 1993

Journal of Neurophysiology

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1. The olfactory processing network in the procerebral (PC) lobe of the terrestrial mollusk Limax maximus exhibits a coherent oscillation of local field potential that is modulated by odor input. To understand the cellular basis of this oscillation, we developed a cell culture preparation of isolated PC neurons and studied the responses of isolated cells to stimulation with neurotransmitters known to be present in the PC lobe. 2. The distribution of PC soma diameters suggests at least two different populations of neurons. Approximately 95% of isolated cells had soma diameters of 7-8 microns, with the remaining cells having larger diameters (10-15 microns). 3. Extracellular measurements of action potentials and optical measurements of intracellular calcium concentrations in fura-2-loaded cells were made. Serotonin and dopamine excited PC neurons and promoted transitions from steady to bursty activity. Both amines elicited increases in intracellular calcium, presumably concomitant with the increase in action-potential frequency. 4. Glutamate suppressed action-potential firing and reduced intracellular calcium. This effect was seen most clearly when glutamate was applied to cells excited by high potassium medium. Quisqualate is an effective glutamate agonist in this system, whereas kainate is not. 5. Combined with anatomic and biochemical data and with studies of the effects of these neurotransmitters on the oscillating local field potential of the intact PC network, the data from isolated PC neurons are consistent with the hypothesis that dopamine and serotonin modulate network dynamics, whereas glutamate is involved in generating the basic oscillation of local field potential in the PC. 6. The optical studies of fura-2-loaded cells showed that several treatments that increase the rate of action-potential production lead to elevations in intracellular calcium. Optical studies of intracellular calcium may be useful for multisite measurements of activity in the intact, oscillating PC lobe network.

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The importance of central noradrenergic influences on the olfactory bulb in the processing of learned olfactory cues

Cited by 67 publications

References 0 publications

Activation of GABAA Receptors in the Accessory Olfactory Bulb Does Not Prevent the Formation of an Olfactory Memory in Mice.

Activation of GABAA Receptors in the Accessory Olfactory Bulb Does Not Prevent the Formation of an Olfactory Memory in Mice.

The influence of chemical complexity on the perception of multicomponent odor mixtures

Cultured olfactory interneurons from Limax maximus: optical and electrophysiological studies of transmitter-evoked responses

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