Dose-dependent nonassociative olfactory learning in a fly

Olfactory sensory stimulation induces a fast-phase arrest response (FPA-R) of the blowfly heart activity that has been described as a sensitive tool for testing insect reactivity to odor perception. We analyzed FPA-R occurrence to repeated olfactory stimulation with low and high 1-hexanol concentrations that are behaviorally attractant and repellent, respectively, in the blowfly. FPA-R occurrence diminished and ceased with repeated presentations of low and medium odor concentrations, according to dynamics inversely related to odor doses. On the other hand, repeated stimulation with higher odor concentrations induced persistent FPA-Rs. Sensory input amplitude to repeated presentations of singly tested odor concentrations did not change throughout stimulation sessions. A spontaneous restoration of FPA-R to olfactory stimulation was recorded 30 min after cessation of FPA-R to a previous olfactory stimulation session. However, a prompt restoration of FPA-R to olfactory stimulation after cessation of FPA-R was obtained following mechano-taste stimulation of labellar sensilla. Our findings show that the FPA-R habituates to olfactory sensory stimulation with low and medium odor concentrations according to dynamics inversely related to odor intensities. On the other hand, the FPA-R does not habituate to higher odor concentrations. Therefore, flies learn to disregard nonaversive odor information, but they cannot ignore iterative detection of a repellent volatile.     

Recording of spontaneous oscillations in the procerebrum of terrestrial mollusk Helix in free behavior

Procerebrum is the central part of the olfactory system in terrestrial snails. Spontaneous rhythmic oscillations were described in this structure. The role of these oscillations in the mechanisms of odor perception and discrimination is unknown yet. Electrical activity of the Helix procerebrum was recorded in vivo. Changes in spontaneous rhythmic oscillations in response to olfactory stimulation were observed. Within the first 10 s after odor application (cineole) in low concentration, a statistically significant decrease in the frequency and increase in the amplitude of procerebrum oscillations were revealed in freely behaving animals. Timing of those changes corresponded to the time of defensive reaction realization of the tentacle withdrawal. The increase in the amplitude and a tendency to a decrease in the frequency of oscillations in response to odor application in high concentration were observed in time period 11-20 s, which corresponded to an increased duration of tentacle withdrawal. The results suggest an implicit relation of the amplitude and frequency of oscillations in odor perception and discrimination.     

Olfactory bulb output cell temporal response patterns to increasing odor concentrations in freely breathing rats

This study compares the single-unit responses of 74 mitral/tufted cells recorded in freely breathing rats to step increases of the intensity of five odorants from 2 x 10(-4) to 10(-1) of saturated vapor pressure. It reveals a stability of the responses of these olfactory bulb output cells. Olfactory stimulation has frequently been shown to produce a strong patterning of mitral/tufted cell discharges highly correlated with respiration. In this study, cells were generally found to show the same response type to two consecutive concentrations, and only a few cells switched their response from excitation to suppression or vice versa. Their firing peak and/or trough occupied the same position in a high proportion of respiratory cycles recorded during a stimulation, and they remained significantly time-locked to the same respiratory epoch for the next higher concentration. Increasing odor concentration did not cause the mean firing frequency of individual cells during a peak to change appreciably between successive or extreme concentrations. By contrast, it tended to shift their maximum frequency during this peak towards an earlier respiratory cycle after stimulation onset. These results are compared with data reported in other electrophysiological studies and with results given by olfactory bulb models before being discussed for their implications in odor coding.      

Olfactory receptor cell responses of pigeon to some odors

A preparation has been developed in the pigeon which allows recording of the electrical activity from an olfactory nerve twig containing the nonmyelinated axons of a small group of olfactory receptor cells. The pigeon's response to n-amylacetate is vigorous and stable, like that of other air-breathing animals. Responses in the olfactory receptor cells in the pigeon increased in magnitude with increase in the odor concentration. An olfactory nerve twig produced a different magnitude of responses to the various odor stimuli. When an odor stimulation was applied to the olfactory mucosa, the two different olfactory nerve twigs which were separated from the same olfactory nerve bundle produced a different magnitude of responses. The differences may be dependent on several factors.     

Electroolfactogram study of the unilaterally axotomized frog

Changes of amplitude in the electroolfactogram (EOG) were investigated following unilateral section of the olfactory nerve. A reduction in EOG amplitude was observed during the first two weeks after the operation; electrical activity gradually began to return to normal and reached 80–100% of control level for trial substances by the end of the third week. Complete disappearance of EOG over the entire surface of the olfactory organ was not observed in any of the animals. A reduction in EOG amplitude was also noted on the unoperated side of the olfactory organ. These changes were less pronounced: the decrease in electrical response level began at a later stage, while complete recovery in amplitude was achieved sooner. Findings showed that EOG amplitude changed at different rates in different areas of the olfactory epithelium; it decreased sooner and began to recover at a later stage in the caudal than in the centromedial portion of the olfactory organ.Institute of Applied Mathematics and Cybernetics, N. I. Lobachevskii University, Gor'kii. Translated from Neirofiziologiya, Vol. 18, No. 5, pp. 603–610, September–October, 1986.     

Origin of basal activity in mammalian olfactory receptor neurons

Mammalian odorant receptors form a large, diverse group of G protein-coupled receptors that determine the sensitivity and response profile of olfactory receptor neurons. But little is known if odorant receptors control basal and also stimulus-induced cellular properties of olfactory receptor neurons other than ligand specificity. This study demonstrates that different odorant receptors have varying degrees of basal activity, which drives concomitant receptor current fluctuations and basal action potential firing. This basal activity can be suppressed by odorants functioning as inverse agonists. Furthermore, odorant-stimulated olfactory receptor neurons expressing different odorant receptors can have strikingly different response patterns in the later phases of prolonged stimulation. Thus, the influence of odorant receptor choice on response characteristics is much more complex than previously thought, which has important consequences on odor coding and odor information transfer to the brain.     

Slow breathing and emotions associated with odor-induced autobiographical memories

An important feature of olfactory perception is its dependence on respiratory activity. By inspiration, olfactory information ascends directly to olfactory-related limbic structures. Therefore, every breath with odor molecules activates these limbic areas associated with emotional experience and memory retrieval. We tested whether odors associated with autobiographical memories can trigger pleasant emotional experiences and whether respiration changes during stimulation with these odors. During presentation of odors related to autobiographical memories and control odors, we measured minute ventilation, tidal volume, respiratory frequency, O2 consumption, and end tidal CO2 concentration. Findings showed that autobiographical memory retrieval was associated with increasing tidal volume and decreasing respiratory frequency more than during presentation of control odors. Subjective feelings such as emotional arousal during retrieval of the memory, arousal level of the memory itself, or pleasantness and familiarity toward the odor evoked by autobiographical memory were more specific emotional responses compared with those related to control odors. In addition, high trait anxiety subjects responded with a stronger feeling of being taken back in time and had high arousal levels with tidal volume increases. We discussed assumptions regarding how deep and slow breathing is related to pleasantness and comfortableness of an autobiographical memory.     

嗅球僧帽细胞具有编码气味空间信息的能力

刺激源的方位是刺激的重要特性之一.行为学的研究发现,动物能够利用气味到达左右鼻腔的时间差和强度差信息对气味方位进行感知,但作为嗅觉系统第一神经中枢的嗅球,是否具有利用两侧鼻间差信息对气味方位进行编码的能力一直受到质疑.为探讨该问题,在本研究中通过比较嗅球中84个僧帽细胞对同侧气味刺激、对侧气味刺激以及对侧气味刺激略先于同侧气味刺激时的反应,发现有29个僧帽细胞可被同侧气味所兴奋,其中18个虽然对对侧气味刺激不反应,但对侧气味的存在却能显著降低其对同侧气味刺激的反应.另外,50个僧帽细胞在只给予同侧或对侧气味刺激时不反应,但其中11个在对侧刺激略先于同侧刺激的方式给出气味时,表现出明显的兴奋性反应.我们的研究结果一方面提示僧帽细胞具有编码气味到达两个鼻腔的时间差,或气味源位置信息的能力;另一方面也表明对侧刺激不仅能对同侧嗅球僧帽细胞产生抑制效应,还可能存在目前还不明确的机制而产生兴奋效应.     

Olfactory interference during inhibitory backward pairing in honey bees

Background

Restrained worker honey bees are a valuable model for studying the behavioral and neural bases of olfactory plasticity. The proboscis extension response (PER; the proboscis is the mouthpart of honey bees) is released in response to sucrose stimulation. If sucrose stimulation is preceded one or a few times by an odor (forward pairing), the bee will form a memory for this association, and subsequent presentations of the odor alone are sufficient to elicit the PER. However, backward pairing between the two stimuli (sucrose, then odor) has not been studied to any great extent in bees, although the vertebrate literature indicates that it elicits a form of inhibitory plasticity.

Methodology/Principal Findings

If hungry bees are fed with sucrose, they will release a long lasting PER; however, this PER can be interrupted if an odor is presented 15 seconds (but not 7 or 30 seconds) after the sucrose (backward pairing). We refer to this previously unreported process as olfactory interference. Bees receiving this 15 second backward pairing show reduced performance after a subsequent single forward pairing (excitatory conditioning) trial. Analysis of the results supported a relationship between olfactory interference and a form of backward pairing-induced inhibitory learning/memory. Injecting the drug cimetidine into the deutocerebrum impaired olfactory interference.

Conclusions/Significance

Olfactory interference depends on the associative link between odor and PER, rather than between odor and sucrose. Furthermore, pairing an odor with sucrose can lead either to association of this odor to PER or to the inhibition of PER by this odor. Olfactory interference may provide insight into processes that gate how excitatory and inhibitory memories for odor-PER associations are formed.     

Rapid encoding and perception of novel odors in the rat

To gain insight into which parameters of neural activity are important in shaping the perception of odors, we combined a behavioral measure of odor perception with optical imaging of odor representations at the level of receptor neuron input to the rat olfactory bulb. Instead of the typical test of an animal's ability to discriminate two familiar odorants by exhibiting an operant response, we used a spontaneously expressed response to a novel odorant—exploratory sniffing—as a measure of odor perception. This assay allowed us to measure the speed with which rats perform spontaneous odor discriminations. With this paradigm, rats discriminated and began responding to a novel odorant in as little as 140 ms. This time is comparable to that measured in earlier studies using operant behavioral readouts after extensive training. In a subset of these trials, we simultaneously imaged receptor neuron input to the dorsal olfactory bulb with near-millisecond temporal resolution as the animal sampled and then responded to the novel odorant. The imaging data revealed that the bulk of the discrimination time can be attributed to the peripheral events underlying odorant detection: receptor input arrives at the olfactory bulb 100–150 ms after inhalation begins, leaving only 50–100 ms for central processing and response initiation. In most trials, odor discrimination had occurred even before the initial barrage of receptor neuron firing had ceased and before spatial maps of activity across glomeruli had fully developed. These results suggest a coding strategy in which the earliest-activated glomeruli play a major role in the initial perception of odor quality, and place constraints on coding and processing schemes based on simple changes in spike rate.     

Testing for Odor Discrimination and Habituation in Mice

This video demonstrates a technique to establish the presence of a normally functioning olfactory system in a mouse. The test helps determine whether the mouse can discriminate between non-social odors and social odors, whether the mouse habituates to a repeatedly presented odor, and whether the mouse demonstrates dishabituation when presented with a novel odor. Since many social behavior tests measure the experimental animal’s response to a familiar or novel mouse, false positives can be avoided by establishing that the animals can detect and discriminate between social odors. There are similar considerations in learning tests such as fear conditioning that use odor to create a novel environment or olfactory cues as an associative stimulus. Deficits in the olfactory system would impair the ability to distinguish between contexts and to form an association with an olfactory cue during fear conditioning. In the odor habitation/dishabituation test, the mouse is repeatedly presented with several odors. Each odor is presented three times for two minutes. The investigator records the sniffing time directed towards the odor as the measurement of olfactory responsiveness. A typical mouse shows a decrease in response to the odor over repeated presentations (habituation). The experimenter then presents a novel odor that elicits increased sniffing towards the new odor (dishabituation). After repeated presentation of the novel odor the animal again shows habituation. This protocol involves the presentation of water, two or more non-social odors, and two social odors. In addition to reducing experimental confounds, this test can provide information on the function of the olfactory systems of new knockout, knock-in, and conditional knockout mouse lines.     

Patterned response to odor in single neurones of goldfish olfactory bulb: influence of odor quality and other stimulus parameters

Responses of 75 single units in the goldfish olfactory bulb were analyzed in detail for their relationship to the time-course of the change in odor concentration during each odor stimulus. Odor stimuli were controlled for rise time, duration, and peak concentration by an apparatus developed for the purpose. This apparatus enabled aqueous odor stimuli to be interposed into a constant water stream without changes in flow rate. The time-course of the concentration change within the olfactory sac was inferred from conductivity measurements at the incurrent and excurrent nostrils. Temporal patterns of firing rate elicited by stimuli with relatively slow rising and falling phases could be quite complex combinations of excitation and suppression. Different temporal patterns were produced by different substances at a single concentration in most units. Statistical measures of the temporal pattern of response for a small number of cells at a given concentration were more characteristic of the stimulus substance than any of three measures of magnitude of response. The temporal patterns change when the peak concentration, duration, and rise time of the stimuli are varied. The nature of these changes suggests that the different patterns are due primarily to the combined influence of two factors: (a) a stimulus whose concentration varies over time and (b) a relationship between concentration and impulse frequency which varies from unit to unit. Some units produce patterns suggestive of influence by neural events of long time constant. The importance of temporal patterns in odor quality and odor intensity coding is discussed.     

Excitatory local interneurons enhance tuning of sensory information

Neurons in the insect antennal lobe represent odors as spatiotemporal patterns of activity that unfold over multiple time scales. As these patterns unspool they decrease the overlap between odor representations and thereby increase the ability of the olfactory system to discriminate odors. Using a realistic model of the insect antennal lobe we examined two competing components of this process -lateral excitation from local excitatory interneurons, and slow inhibition from local inhibitory interneurons. We found that lateral excitation amplified differences between representations of similar odors by recruiting projection neurons that did not receive direct input from olfactory receptors. However, this increased sensitivity also amplified noisy variations in input and compromised the ability of the system to respond reliably to multiple presentations of the same odor. Slow inhibition curtailed the spread of projection neuron activity and increased response reliability. These competing influences must be finely balanced in order to decorrelate odor representations.     

Effects of olfactory peduncle sectioning on the single unit responses of olfactory bulb neurons to odor presentation in awake rabbits

The influences of centrifugal inputs to the olfactory bulb werestudied by recording singlecell responses evoked by olfactorystimuli in intact and peduncle-sectioned bulbs of awake freebreathingrabbits. Responses of intact animals were mainly characterizedby a temporal reorganization of the single unit discharge -responsive second order neurons increased their firing activityduring inspirations and were silent during expirations. Thissynchronization of firing discharge with respiration occurredin the absence of any significant change in the overall firingactivity measured over intervals which included both the inspiratoryand expiratory phases of the respiratory cycle. By contrast,neurons recorded in isolated olfactory bulbs exhibited eithera significant increase or a decrease in firing activity duringodor presentation, and, furthermore, the synchronization ofthese units to the respiratory cycle was markedly reduced comparedwith that in intact animals. Comparison of cell responsivenessbetween intact and isolated olfactory bulbs indicated that thelesion increased the number of odors which induced a response,but did not change the percentage of cells which failed to respondto any of the 5 odorants used in this study. The cell responsivenessincreased for camphor and isoamyl acetate, and to a lesser extentfor food odor. The results indicate that high order nervousstructures exert a powerful inhibitory influence on the responsesof olfactory bulb second-order neurons to odor stimuli. Theyalso suggest that, in intact rabbits, centrifugal inputs playa role in the odor-induced synchronization of the single unitactivity with respiration.     

Neuroethology of olfactory preference development

Young mammals come to approach the odor of their mother, a response that facilitates their survival during early life. Young rats induce a cascade of events in their mother to induce the emission of her odor. The pups increase circulating prolactin levels, which increases food intake and the emission of large quantities of cecotrophe containing the maternal odor. This odor is synthesized by the action of cecal microorganisms and changes with maternal diet. The diet-dependence of the odor requires the pups to acquire their attraction to the odor postnatally. The acquisition of this preference occurs when an odor is paired with the tactile stimulation that pups receive during maternal care. The action of the tactile stimulation appears to be mediated by noradrenaline. The development of this type of olfactory attraction is accompanied by changes in the regions of the olfactory bulb that are responsive to the attractive odor. Metabolic, anatomical, and neurophysiological changes in response to the attractive odor emerge in such regions of the bulb after early olfactory preference training. © 1992 John Wiley & Sons, Inc.     

Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly

Three classes of neurons form synapses in the antennal lobe of Drosophila, the insect counterpart of the vertebrate olfactory bulb: olfactory receptor neurons, projection neurons, and inhibitory local interneurons. We have targeted a genetically encoded optical reporter of synaptic transmission to each of these classes of neurons and visualized population responses to natural odors. The activation of an odor-specific ensemble of olfactory receptor neurons leads to the activation of a symmetric ensemble of projection neurons across the glomerular synaptic relay. Virtually all excited glomeruli receive inhibitory input from local interneurons. The extent, odor specificity, and partly interglomerular origin of this input suggest that inhibitory circuits assemble combinatorially during odor presentations. These circuits may serve as dynamic templates that extract higher order features from afferent activity patterns.     

Neuroethology of olfactory preference development.

Young mammals come to approach the odor of their mother, a response that facilitates their survival during early life. Young rats induce a cascade of events in their mother to induce the emission of her odor. The pups increase circulating prolactin levels, which increases food intake and the emission of large quantities of cecotrophe containing the maternal odor. This odor is synthesized by the action of cecal microorganisms and changes with maternal diet. The diet-dependence of the odor requires the pups to acquire their attraction to the odor postnatally. The acquisition of this preference occurs when an odor is paired with the tactile stimulation that pups receive during maternal care. The action of the tactile stimulation appears to be mediated by noradrenaline. The development of this type of olfactory attraction is accompanied by changes in the regions of the olfactory bulb that are responsive to the attractive odor. Metabolic, anatomical, and neurophysiological changes in response to the attractive odor emerge in such regions of the bulb after early olfactory preference training.     

Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera

Mushroom bodies are central brain structures and essentially involved in insect olfactory learning. Within the mushroom bodies γ-aminobutyric acid (GABA)-immunoreactive feedback neurons are the most prominent neuron group. The plasticity of inhibitory neural activity within the mushroom body was investigated by analyzing modulations of odor responses of feedback neurons during olfactory learning in vivo. In the honeybee, Apis mellifera, feedback neurons were intracellularly recorded at their neurites. They produced complex patterns of action potentials without experimental stimulation. Summating postsynaptic potentials indicate that their synaptic input region lies within the lobes. Odor and antennal sucrose stimuli evoked excitatory phasic-tonic responses. Individual neurons responded to various odors; responses of different neurons to the same odor were highly variable. Response modulations were determined by comparing odor responses of feedback neurons before and after one-trial olfactory conditioning or sensitisation. Shortly after pairing an odor stimulus with a sucrose reward, odor-induced spike activity of feedback neurons decreased. Repeated odor stimulations alone, equally spaced as in the conditioning experiment, did not affect the odor-induced excitation. A single sensitisation trial also did not alter odor responses. These findings indicate that the level of odor-induced inhibition within the mushroom bodies is specifically modulated by experience. Accepted: 9 September 1999     

Faster, deeper, better: the impact of sniffing modulation on bulbar olfactory processing

A key feature of mammalian olfactory perception is that sensory input is intimately related to respiration. Different authors have considered respiratory dynamics not only as a simple vector for odor molecules but also as an integral part of olfactory perception. Thus, rats adapt their sniffing strategy, both in frequency and flow rate, when performing odor-related tasks. The question of how frequency and flow rate jointly impact the spatio-temporal representation of odor in the olfactory bulb (OB) has not yet been answered. In the present paper, we addressed this question using a simulated nasal airflow protocol on anesthetized rats combined with voltage-sensitive dye imaging (VSDi) of odor-evoked OB glomerular maps. Glomerular responses displayed a tonic component during odor stimulation with a superimposed phasic component phase-locked to the sampling pattern. We showed that a high sniffing frequency (10 Hz) retained the ability to shape OB activity and that the tonic and phasic components of the VSDi responses were dependent on flow rate and inspiration volume, respectively. Both sniffing parameters jointly affected OB responses to odor such that the reduced activity level induced by a frequency increase was compensated by an increased flow rate.