Flavor-illness aversions: the role of the amygdala in the acquisition of taste-potentiated odor aversions

In the present experiments the role of the amygdaloid complex and its specific nuclei were tested in the conditioning of taste potentiated odor aversions. In the first experiment two groups of rats were given either large electrolytic lesions in the amygdala (AMX) or sham operations (SH). Postoperatively, these rats were trained to avoid either a taste, an odor, or a taste-odor compound using LiCl illness. Subsequent tests with odor and taste alone showed that the SH group developed strong taste and odor aversions; however, the AMX group failed to display either an odor or taste aversion. In the second experiment, another four groups of rats received either lesions in the medial and basomedial nuclei (M), central nuclei (C), lateral and basolateral (L), or sham operations (SH). The results from postoperative conditioning showed that all groups had strong taste and odor aversions, except group L which displayed a significant disruption of odor aversion learning. In conclusion, these data indicate that the amygdala is involved in the acquisition of taste, odor and potentiated odor aversions learning. Moreover, it is demonstrated that the lateral and/or basolateral nuclei are particularly involved in the development of potentiated odor aversions learning.     

Effects of brain lesions on taste-potentiated odor aversion in rats

Rats failed to acquire aversions to odor stimulus, which was followed 30 min later by an unconditioned stimulus (US). However, when the odor stimulus was accompanied by a taste stimulus, they acquired odor aversions as well as taste aversions. In this phenomenon, referred to as a taste-potentiated odor aversion, lesions of the amygdala disrupted both taste and odor aversions, whereas lesions of the parvicellular part of ventroposteromedial thalamic nucleus (VPMpc) or insular cortex (IC) disrupted taste aversion but attenuated only odor aversion. These results suggest that both taste and odor stimuli are associated with US in the amygdala and that taste inputs delivered to the amygdala through the IC and/or VPMpc play an important role in potentiation of odor aversion. ((c) 2006 APA, all rights reserved).     

Involvement of the anterior insular gustatory neocortex in taste-potentiated odor aversion learning

When an odor conditioned stimulus (CS) precedes illness (unconditioned stimulus; UCS), rats acquire relatively weak odor aversions. Conversely, when a compound odor-taste (flavor) CS precedes illness, rats acquire robust aversions both to the odor and to the taste components of a compound flavor CS. Thus, tastes potentiate odor-illness aversions during toxiphobic conditioning. Such conditioning effects have been referred to as taste-potentiated odor aversion learning (POA). Previous neurobehavioral experiments have shown that the anterior insular gustatory neocortex contributes to conditioned taste aversion (CTA) learning. The present experiment examined the involvement of the anterior insular gustatory neocortex in CTA learning and POA learning. To that end, four distinct groups of rats received bilateral electrolytic lesion placements in the orbitofrontal neocortex, the "somatic" gustatory neocortex, the anterior insular gustatory neocortex or the posterior insular neocortex. Control animals received anesthesia only. Subgroups of animals thereafter received aversion conditioning using either an odor (almond) CS or a compound odor-taste (almond-saccharin) CS. Aversions to the almond odorant and/or saccharin tastant were evaluated during extinction. Results indicated that animals lacking orbitofrontal neocortex or posterior insular neocortex acquired normal CTAs and POAs. Animals lacking somatic gustatory neocortex exhibited impaired CTA learning, yet those animals showed normal POA learning. Lesions centered in the anterior insular neocortex impaired both CTA learning and POA learning. These results demonstrate that the insular gustatory neocortex is uniquely involved in the higher-order integration of odors, tastes and illness.     

Preexposure and extinction effects of lithium chloride induced taste-potentiated aversions for spatially contiguous auditory food cues in rats

Taste potentiated illness-induced aversions for noisy food were studied in Sprague-Dawley rats. The rats ate from receptacles containing salty food and a contiguous tone produced by speakers under the food followed by lithium chloride injections. In preference tests, the rats then avoided noisy food in favor of quiet food followed by extinction and spontaneous recovery of the auditory aversion over repeated nonreinforced trials. Other rats were given either 4 or 10 days of exposure to the noisy food prior to taste-toxicosis treatment. None of these rats subsequently avoided noisy food. The importance of spatial contiguity and methodological variation in associating nongustatory food cues with illness is discussed.     

Basolateral amygdala NMDA receptors are selectively involved in the acquisition of taste-potentiated odor aversion in the rat

In the taste-potentiated odor aversion (TPOA) paradigm, animals acquire a strong aversion to an odor that is followed by delayed intoxication only if a gustatory stimulus is presented with the odor during conditioning. Although previous work has shown that N-methyl-D-aspartate (NMDA) receptors in the basolateral nucleus of the amygdala (BLA) play a role in the acquisition of TPOA, the present study aimed at describing the process in which NMDA receptors in the BLA are involved during acquisition of TPOA. Male Long-Evans rats received intra-BLA infusions of the competitive NMDA receptor antagonist D,L-2-2-amino-5-phosphonovalerate (D-APV; 0.05 and 0.50 microg) immediately before or after the odor-taste conditioned stimulus (CS) presentation, or immediately before the test. Results showed that D-APV impaired acquisition of TPOA when infused before, but not after, the CS presentation, but did not affect retrieval. These results suggest that NMDA receptors of the BLA are involved in the formation of potentiation--by taste--of the olfactory memory trace, but not in the maintenance of this process.     

The effect of amygdala-kindled seizures on the acquisition of taste and odor aversions

Two experiments were conducted to investigate the effect of amygdala-kindled seizures on the acquisition of fluid aversions using taste, odor, and compound taste-odor cues. In Experiment 1 all subjects were poisoned with lithium chloride 30 minutes after ingesting a novel taste. Experimental subjects were either kindled 15 minutes following ingestion or 15 minutes following LiCl injection. The strength of the taste aversion in the kindled animals was significantly attenuated compared to nonkindled controls. There was a tendency for kindling within the CS-US interval to be more disruptive than kindling that occurred after LiCl injection. The second study explored the effect of kindling after the CS on the development of aversions to an odor cue or a compound taste-odor cue. This study found that kindling after drinking effectively blocked the acquisition of both odor and taste aversions and compounding did not affect the strength of the odor aversion.     

Quality and intensity of binary odor mixtures

The perceived intensity and quality of binary mixtures consisting of the common but dissimilar odorants, benzaldehyde (almond), eugenol (cloves), propionic acid (vinegar) and (-)-carvone (spearmint), were determined over a wide range of environmentally relevant concentrations. Consistent data were obtained from each of the odor pairs. This showed that the intensity of odorants not their quality determined the contribution of each to the quality of a mixture. Except for the pair carvone-propionic acid, both odorants were perceived only when the difference between their intensities was small. The results confirmed an earlier finding that the total intensity of a mixture is less than the sum of the intensities of the two components, and also showed that it is never less than the intensity of the weaker component. Seven major characteristics of binary odor mixtures are defined.     

Effect of odor quality and intensity on conditioned odor aversion learning in the rat

Odor quality and intensity were varied to test the ability of rats to associate odor with an induced illness. Rats were allowed 10 minutes access to water on each of nine days; deodorized air was directed towards each rat's nose while drinking at familiarization and recovery sessions (days 1-5 and 7-8, respectively) and odorized air at treatment and test sessions (days 6 and 9, respectively). Each rat was injected with LiCl following its drinking period on day 6. The difference between the amount of water consumed on day 6 and day 9 gave a measure of the conditioned aversion. Only mild or no aversion occurred with odors of n-butyric acid, benzylamine, cyclohexanone, and n-butanol. Strong conditioned aversions were obtained to odors of triethylamine, 1,4-cineole, and isoamyl acetate, and the degree of aversion increased linearly with the log of odor concentration. The effect of odor quality, intensity and presentation method, and the role of the different chemoreceptor systems in the acquisition of odor aversions are discussed.     

Optimum perception of odor intensity by humans

The sniff duration that provides optimum perception of odor intensity was determined for 17 humans. Subjects were trained to match the duration of their sniff to the duration of a buzzer that sounded for 0.2, 0.5, 1.0 or 2.0 sec. Sniff characteristics were monitored with a hot wire anemometer and an oscilloscope. Intensity estimates were obtained at the four durations for three concentrations of phenyl ethanol, butanol and propionic acid. Optimum perception of intensity occurred between 0.39 and 0.64 sec for phenyl ethanol and propionic acid and a value of no more than 1.63 sec is proposed for butanol. The longer duration for butanol is attributed to the delayed response of nerves in the throat which appear to respond to this odorant but not to the others. The complexity of the intensity sensation and implications of the results for neurophysiological studies of intensity coding are discussed and the properties of an olfactometer for odor intensity measurements are outlined.     

Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study

The primary olfactory brain center, the antennal lobe (AL) in insects or the olfactory bulb in vertebrates, is a notable example of a neural network for sensory processing. While physiological properties of the input, the olfactory receptor neurons, have become clearer, the operation of the network itself remains cryptic. Therefore we measured spatio-temporal odor-response patterns in the output neurons of the olfactory glomeruli using optical imaging in the honeybee Apis mellifera. We mapped these responses to identified glomeruli, which are the structural and functional units of the AL. Each odor evoked a complex spatio-temporal activity pattern of excited and inhibited glomeruli. These properties were odor- and glomerulus-specific and were conserved across individuals. We compared the spatial pattern of excited glomeruli to previously published signals, which derived mainly from the receptor neurons, and found that they appeared more confined, showing that inhibitory connections enhance the contrast between glomeruli in the AL. To investigate the underlying mechanisms, we applied GABA and the GABA-receptor antagonist picrotoxin (PTX). The results show the presence of two separate inhibitory networks: one is GABAergic and modulates overall AL activity, the other is PTX-insensitive and glomerulus-specific. Inhibitory connections of the latter network selectively inhibit glomeruli with overlapping response profiles, in a way akin to "lateral" inhibition in other sensory systems. Selectively inhibited glomeruli need not be spatial neighbors. The net result is a globally modulated, contrast-enhanced and predictable representation of odors in the olfactory output neurons.     

Taste potentiation of poisoned odor by temporal contiguity

The synergistic interaction between odor and taste in flavor-toxicosis conditioning was tested in two experiments. The temporal interval between a 2-min odor and a 2-min taste was varied for thirsty rats licking at a water spout. In the first experiment, taste was presented at time zero, and odor was presented at -10, -1, 0, 1 and 10 min to independent groups in a simple compartment. In the second experiment, taste was presented at 0, and odor was presented at -5, -2, and 0 min in a "wind tunnel" apparatus. The results indicated that odor alone is an ineffective conditioned stimulus for a toxic unconditioned stimulus under our conditions, simultaneous (0-min) presentation of odor with taste potentiates the odor component so that it becomes more effective than the taste component, a 2-min interval between odor and taste attenuates potentiation, and a 5-min interval disrupts the effect, and the interaction in asymmetrical, that is, odor has no such systematic effect on the conditioning of taste.     

A measure of taste intensity discrimination in the rat through conditioned taste aversions

The ability of rats to make intensity discriminations was determined by forming a conditioned taste aversion to a moderate concentration of each of four basic taste stimuli, and then measuring the level of acceptance (number of licks during a 15 sec exposure) shown to a range of concentrations of the same chemical. Rats (N = 66) could discriminate between glucose concentrations that were separated by as little as 0.074 M, between NaCl concentrations that differed by 0.029 M, between HCl concentrations that were 9 X 10(-4) M apart, and between quinine HCl concentrations that differed by as little as 2.4 X 10(-6) M.     

Visuotactile temporal order judgments in ageing

We report an experiment on the effects of ageing on crossmodal temporal perception. Young (mean age = 21.7 years) and old (mean age = 75.1 years) participants were presented with pairs of visual and vibrotactile stimuli to either hand and required to make unspeeded temporal order judgments (TOJs) regarding which sensory modality appeared to have been presented first. The stimulus onset asynchrony (SOA) between the two stimuli was varied using the method of constant stimuli. Temporal precision, as indexed by the just noticeable difference (JND), was better (i.e., JNDs were lower) when the stimuli were presented from different positions (M = 101 ms) rather than from the same position (M = 120 ms), as has been demonstrated previously. Additionally, older observers required more time (i.e., their JNDs were larger) to accurately perceive the temporal order (M = 131 ms) as compared to younger observers (M = 98 ms). Our results confirm that ageing deleteriously affects crossmodal temporal processing even when the spatial confound inherent in previous research has been ruled out.     

Consolidation of temporal order in episodic memories

Even though it is known that sleep benefits declarative memory consolidation, the role of sleep in the storage of temporal sequences has rarely been examined. Thus we explored the influence of sleep on temporal order in an episodic memory task followed by sleep or sleep deprivation. Thirty-four healthy subjects (17 men) aged between 19 and 28 years participated in the randomized, counterbalanced, between-subject design. Parameters of interests were NREM/REM cycles, spindle activity and spindle-related EEG power spectra. Participants of both groups (sleep group/sleep deprivation group) performed retrieval in the evening, morning and three days after the learning night. Results revealed that performance in temporal order memory significantly deteriorated over three days only in sleep deprived participants. Furthermore our data showed a positive relationship between the ratios of the (i) first NREM/REM cycle with more REM being associated with delayed temporal order recall. Most interestingly, data additionally indicated that (ii) memory enhancers in the sleep group show more fast spindle related alpha power at frontal electrode sites possibly indicating access to a yet to be consolidated memory trace. We suggest that distinct sleep mechanisms subserve different aspects of episodic memory and are jointly involved in sleep-dependent memory consolidation.     

Ontogenetic comparison of memory for Pavlovian conditioned aversions to temperature, vibration, odor, or brightness

Ontogenetic differences in forgetting of Pavlovian conditioning were tested in four experiments with 550 rats of ages 12, 18, or 60 days postpartum. The experiments had in common the same unconditioned stimulus (US; footshock) and procedures for conditioning and testing, but the conditioned stimulus (CS) differed. The CS was a particular vibrotactile stimulus (Experiment 1), ambient temperature (Experiment 2), odorant (Experiment 3), or brightness (Experiment 4). The intent of this study was to assess, in more comparable circumstances than previously tested, the possibility of substantial differences in infantile amnesia for different sensory modalities. Particular attention was given those modalities that mature early and had not been tested in previous studies of infantile amnesia. The results verified some degree of infantile amnesia for even those sensory modalities used adaptively from birth.     

Interaction of intensity and order regarding painful events

While stimulus intensity obviously affects degree of pain responding, presentation order effects of stimuli of different intensities on acute pain responses are under-researched. The present study examined the effects of manipulating presentation order of lower and higher pain stimulus intensity. Using 96 undergraduates, this investigation employed a 2 × 2 mixed research design, with pain stimulus sequence as a between-subjects variable and pain stimulus trial as a repeated measure. When the greater pain stimulus intensity was presented last, verbal report of pain was higher. Also, performance of a cognitive task was interrupted the least when the lower stimulus intensity was presented last. Heart rate, however, was highest when the greater stimulus intensity was presented first, and pain tolerance was greatest when the lower stimulus intensity was presented first. Results are discussed in relation to adaptation-level effects, and implications for pain experienced in clinical settings are suggested.

Normal aging and odor intensity effects on the olfactory event-related potential.

Olfactory event-related potentials (OERPs) were recorded in 14 young and 14 older adults, with odor strength of isoamyl acetate manipulated to assess olfactory stimulus intensity. Young participants produced significantly larger N1/P2, N2/P3 amplitudes and shorter N1, P2 and N2 latencies than older participants. Medium- and high-odor concentrations elicited significantly shorter P2 and N2 latencies than the lowest concentration for both age groups. Odor concentration appears to affect the speed of olfactory stimulus information processing regardless of age.     

Patterned response to odor in mammalian olfactory bulb: the influence of intensity

Responses of single neurons in the olfactory bulb of anesthetized hamsters were recorded extracellularly while odors of defined concentration and time course were delivered to the olfactory system at constant flow. Responses could be either excitatory or suppressive, as judged by the first distinguishable change in firing rate during odor delivery. However, when the time course of the response was examined in more detail, approximately one-third of all tests and one-half of the tests at high concentration resulted in complex temporal patterns of firing rate that involved both increases and decreases with respect to spontaneous activity. Approximately two-thirds of all tests produced responses where increased firing rate preceded any distinguishable suppression. Excitatory and suppressive responses were each classified into four groups according to their temporal patterns. Different patterns were not equally represented in the data and the proportions of patterns elicited by the same odor changed with stimulus intensity. Complex responses, where temporal patterns included periods of firing rate above and below spontaneous rate, were increasingly common and intensity was increased. Magnitude of response is difficult to define when a single response includes both increases and decreases of firing rate but more than half of the neurons that responded to more than one stimulus concentration clearly had nonmonotonic intensity-response functions. Forty-one out of 101 neurons were classified as output cells because they could be driven at short constant latency by lateral olfactory tract stimulation. Their responses were not clearly different from the remaining cells that could not be classified as output cells. The contribution of the inhibitory circuits of the olfactory bulb to the generation of patterned response and to changes in pattern with intensity are discussed. The lateral inhibitory circuits of the bulb appear to be sufficient to explain the data presented here.     

Audiovisual temporal adaptation of speech: temporal order versus simultaneity judgments

The temporal perception of simple auditory and visual stimuli can be modulated by exposure to asynchronous audiovisual speech. For instance, research using the temporal order judgment (TOJ) task has shown that exposure to temporally misaligned audiovisual speech signals can induce temporal adaptation that will influence the TOJs of other (simpler) audiovisual events (Navarra et al. (2005) Cognit Brain Res 25:499–507). Given that TOJ and simultaneity judgment (SJ) tasks appear to reflect different underlying mechanisms, we investigated whether adaptation to asynchronous speech inputs would also influence SJ task performance. Participants judged whether a light flash and a noise burst, presented at varying stimulus onset asynchronies, were simultaneous or not, or else they discriminated which of the two sensory events appeared to have occurred first. While performing these tasks, participants monitored a continuous speech stream for target words that were either presented in synchrony, or with the audio channel lagging 300 ms behind the video channel. We found that the sensitivity of participant’s TOJ and SJ responses was reduced when the background speech stream was desynchronized. A significant modulation of the point of subjective simultaneity (PSS) was also observed in the SJ task but, interestingly, not in the TOJ task, thus supporting previous claims that TOJ and SJ tasks may tap somewhat different aspects of temporal perception.

Visual temporal order judgment in profoundly deaf individuals

We investigated temporal processing in profoundly deaf individuals by testing their ability to make temporal order judgments (TOJs) for pairs of visual stimuli presented at central or peripheral visual eccentricities. Ten profoundly deaf participants judged which of the two visual stimuli appearing on opposite sides of central fixation was delivered first. Stimuli were presented either symmetrically, at central or peripheral locations, or asymmetrically (i.e. one central and the other peripheral) at varying stimulus onset asynchronies (SOAs) using the method of constant stimuli. Two groups of hearing controls were also tested in this task: 10 hearing controls auditory-deprived during testing and 12 hearing controls who were not subjected to any deprivation procedure. Temporal order thresholds (i.e. just noticeable differences) and points of subjective simultaneity for the two visual stimuli did not differ between groups. However, faster discrimination responses were systematically observed in the deaf than in either group of hearing controls, especially when the first of the two stimuli appeared at peripheral locations. Contrary to some previous findings, our results show that a life-long auditory deprivation does not alter temporal processing abilities in the millisecond range. In fact, we show that deaf participants obtain similar temporal thresholds to hearing controls, while also responding much faster. This enhanced reactivity is documented here for the first time in the context of a temporal processing task, and we suggest it may constitute a critical aspect of the functional changes occurring as a consequence of profound deafness.