Role of verbal encoding in shortand long-term odor recognition

The role of verbal encoding in odor recognition memory was investigated using odors of low familiarity to subjects before the experiment began. The experimental procedure included two phases—odor learning (first phase) and odor memory testing (second phase)—separated by a delay of 7 days. Five experimental conditions were established: three conditions of odor learning with names (labeling conditions), one condition of odor learning without names (sensory familiarization), and one condition of no learning prior to testing (control conditions). The labeling conditions differed from each other regarding label characteristics. The names were those of odor sources (veridical names), those personally generated by subjects (generated names), or those derived from the chemical names of the odorants (chemical names). Subjects were required to learn 20 fixed associations between odors (targets or distractors) and 20 names during two daily sessions. The learning sessions included two identification tests and ended by a verbal memory test in which subjects recalled odor names. The odor memory test was split into two parts separated by a retention interval of either 20 min (short-term memory) or 24 h (long-term memory). Data showed that olfactory recognition memory was enhanced in subjects who associated veridical or generated names to odors during the learning session. Chemical names were not appropriate to facilitate odor recognition. Similarly, the level of odor identification was higher for veridical and generated names than for chemical names, though the level of verbal memory for chemical names was substantial. Recognition response latencies were systematically longer for a target odor implying a positive response than for a distractor odor implying a negative response. Together, these data suggest that odor recognition and identification are sensitive to the semantic content of labels associated with odors. Odor memory was adversively influenced by time, but this influence was less pronounced when the names were endowed with a rich semantic content.     

Context specificity of operant discrimination performance in pigeons

In an experiment designed to investigate odors as potential retrieval cues in pigeons' memory (i.e., as conditional stimuli), 8 pigeons first learned to peck a red keylight (S+, reinforced) and not a blue one (S−, extinguished) in the presence of either a eucalyptus oil or isoamyl acetate odor. They were repeatedly switched between two chambers with the same odor to habituate any reaction to the switching that would be required for eventual testing for conditional control by the odors. Next, the birds learned the reversal (blue S+, red S−) in the presence of the alternative odor in one of these chambers. When the birds were then switched to the alternative chamber for additional training, although the odor was still appropriate to the reversal problem, behavior appropriate to the original training condition recurred. Testing indicated that reversal performance was specific to the one chamber in which it had been trained.     

Perceptual learning with odors: implications for psychological accounts of odor quality perception

After two odors have been experienced in a mixture, the pair are subsequently rated as sharing more qualities and smelling more alike than equally exposed controls. These effects may result from the retrieval of a common mixture memory when either component is sniffed alone. If correct, odor pairs experienced together in a mixture should also be less discriminable than those experienced an equal number of times but in different mixtures. This was tested here by exposing participants to two odor mixtures (either AX, BY or AY, BX) and then testing their ability to discriminate between the components. As predicted, odors previously experienced together as a mixture were less discriminable than controls. These and related findings noted above suggest that learning and memory play an important role in odor quality perception.     

Implicit and explicit memory for odors: Hemispheric differences

In two experiments, implicit and explicit tests were used to investigate the lateralization of odor memory. Odors were at all times presented monorhinically. At test, odors were presented to either the ipsi- or the contralateral side of the nostril used for inspection. In Experiment 1, participants were first primed to a set of odors. At test, response latencies for odor identification were measured. The results were that priming odors tested via the left but not the right nostril were identified faster than control odors. In Experiment 2, a similar design probed episodic recognition memory. Memory performance did not differ between the left and right nostrils, but the measures of response latency favored the right side. The study demonstrates that it is possible to tap differences in memory performance between the cerebral hemispheres through monorhinic presentation of odors in healthy persons, and that these differences depend on the test nostril rather than the inspection nostril.     

The involvement of the orbitofrontal cortex in learning under changing task contingencies

Previous investigations examining the rat prefrontal cortex subregions in attentional-set shifting have commonly employed two-choice discriminations. To better understand how varying levels of difficulty influence the contribution of the prefrontal cortex to learning, the present studies examined the effects of orbitofrontal cortex inactivation in a two- or four-choice odor reversal learning test. Long-Evans rats were trained to dig in cups that contained distinct odors. In the two-choice odor discrimination, one odor cup was always associated with a cereal reinforcement in acquisition while the opposite odor cup was associated with a cereal reinforcement in reversal learning. In the four-choice odor discrimination, an additional two cups containing distinct odors were used that were never associated with reinforcement in acquisition or reversal learning. Bilateral infusions of the GABA-A agonist, muscimol (0.5 microg) into the orbitofrontal cortex did not impair acquisition of either the two- or four-choice discrimination task. However, muscimol infusions into the orbitofrontal cortex impaired two- and four-choice reversal learning. In the two-choice odor reversal, muscimol treatment selectively increased perseverative errors. In the four-choice odor reversal, muscimol treatment increased perseverative, regressive, as well as irrelevant errors. These findings suggest that the orbital prefrontal cortex not only enables task switching by supporting the initial inhibition of a previously relevant choice pattern, but under increasing task demands also enables the reliable execution of a new choice pattern and reduction of interference to irrelevant stimuli.     

Memory for instances and categories in children and adults

College subjects and 7-year-olds were trained in sorting 16 words into two conceptual categories. Training consisted of either three list presentations (Experiment I) or training to solution (Experiment II). Then either immediately or after a 3 to 4 week delay subjects received a recognition test which assessed memory for the instance vs categorical properties of the task stimuli by embedding words from the original list and from the list categories with confusion items from either the same or different categories as those on the original list. The data indicated that learning and memory were controlled primarily by categorical properties of the task items in adults and by specific instance properties in children. However, there was evidence that children had learned the categorical attributes of the task and may have differed from adults chiefly in their failure to utilize these attributes to assist learning and memory performance. The age differences in learning and memory were independent of the degree of initial training.     

Reintroduction of Odor Combined with Cognitive Stimulation Supports Creative Ideation via Memory Retrieval Mechanisms

Brainstorming is a widely used method for generating creative ideas. There is an interest in various techniques contributing to it; nevertheless, research examining the influence of an aromatic odor as a facilitator has been scarce. Two experiments were conducted for this purpose. In Experiment I, a mandarin odor was presented with either stimulating (relevant) or non-stimulating (irrelevant) words prior to the brainstorming session, then re-presented during it. The findings showed that re-presenting the odor during brainstorming increased flexible and unique ideas through retrieval of stimulating words from memory. Flexibility also played a mediator role between mandarin odor and unique ideas. In Experiment II, odor presentation times were changed. It was presented prior to brainstorming, during it or both. The first odor presentation enhanced idea generation only when there was a second odor presentation. The findings suggested that it was the combination of the odors, presented before (and alongside a list of stimulating words) and during brainstorming, that contributed to the use of stimulating words during brainstorming. These two experiments revealed the role of mandarin odor on flexible thinking and idea generation via memory retrieval. Moreover, the odor increased recalling performance, even when the stimuli were given implicitly and recently learned.     

Cycloheximide produces amnesia for extinction and reconsolidation in an appetitive odor discrimination task in rats

A considerable literature has shown deficits in memory resulting from the administration of protein synthesis inhibitors; however, most of the past literature in this field has focused on acquisition of new memory using aversively-motivated tasks. The effect of protein synthesis inhibition on appetitive learning and memory as well as extinction is less clear. The present study employed an appetitive odor discrimination paradigm to examine the effects of acute cycloheximide administration (1 mg/kg) on reconsolidation and extinction.Male, Long-Evans adult rats were trained to discriminate between two odors (i.e., cocoa and cinnamon) and then received extinction trials following an intraperitoneal injection of cycloheximide or vehicle. Twenty-four hours later, rats were tested via one non-reinforced test trial. Results showed amnesia for extinction as well as original training (i.e., correct odor choice) in cycloheximide-injected rats in this appetitive task, while vehicle-injected controls showed good memory for extinction. These data add to a growing literature showing the importance of protein synthesis inhibition for extinction and reconsolidation in appetitive learning and memory.     

Very long-term memory for odors: retention of odor-name associations.

The ability to remember odor-name associations for recent odors (those associated with everyday products experienced within the past 2 years) and distant odors (those associated with children's toys not encountered for 3 years or more) was examined in two experiments. In recognition tasks, subjects attempted to match odor names to odors, or odors to odor names. In a recall task, subjects tried to identify odors by name. The results showed that although odor retention was better for recent than distant odors, significant retention remains for odors not experienced since childhood. These results are consistent with other studies that found very slow and gradual loss of odor information in memory. They extend that research by showing that odor information is still available over a much longer period of time.     

Recognition memory for social and non-social odors: differential effects of neurotoxic lesions to the hippocampus and perirhinal cortex

The contributions of the hippocampus (HC) and perirhinal cortex (PER) to recognition memory are currently topics of debate in neuroscience. Here we used a rapidly-learned (seconds) spontaneous novel odor recognition paradigm to assess the effects of pre-training N-methyl-D-aspartate lesions to the HC or PER on odor recognition memory. We tested memory for both social and non-social odor stimuli. Social odors were acquired from conspecifics, while non-social odors were household spices. Conspecific odor stimuli are ethologically-relevant and have a high degree of overlapping features compared to non-social household spices. Various retention intervals (5 min, 20 min, 1h, 24h, or 48 h) were used between study and test phases, each with a unique odor pair, to assess changes in novelty preference over time. Consistent with findings in other paradigms, modalities, and species, we found that HC lesions yielded no significant recognition memory deficits. In contrast, PER lesions caused significant deficits for social odor recognition memory at long retention intervals, demonstrating a critical role for PER in long-term memory for social odors. PER lesions had no effect on memory for non-social odors. The results are consistent with a general role for PER in long-term recognition memory for stimuli that have a high degree of overlapping features, which must be distinguished by conjunctive representations.     

Scopolamine enhances generalization between odor representations in rat olfactory cortex

Acetylcholine (ACh) has a critical, modulatory role in plasticity in many sensory systems. In the rat olfactory system, both behavioral and physiological data indicate that ACh may be required for normal odor memory and synaptic plasticity. Based on these data, neural network models have hypothesized that ACh muscarinic receptors reduce interference between learned cortical representations of odors within the piriform cortex. In this study, odor receptive fields of rat anterior piriform cortex (aPCX) single-units for alkane odors were mapped before and after either a systemic injection of the muscarinic receptor antagonist scopolamine (0.5 mg/kg) or aPCX surface application of 500 μM scopolamine (or saline/ACSF controls). Cross-habituation between alkanes differing by two to four carbons was then examined following a 50-sec habituating stimulus. The results demonstrate that neither aPCX spontaneous activity nor odor-evoked activity (receptive field) was affected by scopolamine, but that cross-habituation in aPCX neurons was enhanced significantly by either systemic or cortical scopolamine. These results indicate that scopolamine selectively enhances generalization between odor representations in aPCX in a simple memory task. Given that ACh primarily affects intracortical association fibers in the aPCX, the results support a role for the association system in odor memory and discrimination and indicate an important ACh modulatory control over this basic sensory process.     

Implicit and explicit tests of odor memory reveal different outcomes following interference

Experiencing two odors as a mixture can later increase their perceived similarity when presented separately. Such an increase in similarity can be used as an implicit measure of how well participants remember the mixture. Three experiments tested the resistance to interference of this effect by first giving participants exposure to two 2-odor mixtures and then presenting each odor from one mixture (interfered pair) separately many times. After the latter interference phase, participants rated the similarity of the two odors in each pair. The experiments varied in terms of the number of initial exposures to the mixtures, the number of odor presentations in the interference phase, and the control conditions employed. No difference in similarity ratings for the interfered and non-interfered pair was found in any experiment. In contrast to the lack of interference with this implicit measure, an explicit measure of memory based on participants’ ratings of odor frequency revealed that they could recall to some degree that the interfered odors had been presented alone in the second phase. These results suggest that implicit memory for odor mixtures is highly resistant to interference and is consistent with a configural encoding account of this effect.     

Recognition of odors and identification of sources

The purpose of the present study was to investigate the accuracy of the memory for odors and for the location of odors. In Experiment 1, 5 unfamiliar odors were presented in each of 2 rooms. Twenty participants were instructed to remember only the odors (odor-only control group) and 20 were instructed to remember both the odors and the room where the odors were presented (odor place group). In Experiment 2, both the odor presentation room and the sex of the experimenters were manipulated to increase the uniqueness of the odor location. The results demonstrated that the memory for an odor is superior to the memory for the location of an odor. The results also indicated that the intention to learn the sources of an odor improves the memory for the source. These results are discussed in the context of the source monitoring framework.     

The role of the dorsal and ventral hippocampus in olfactory working memory

Olfactory working memory and pattern separation for odor information was assessed in male rats using a matching-to-sample for odors paradigm. The odor set consisted of a five aliphatic acids with unbranched carbon chains that varied from two- to six-carbons in length. Each trial consisted of a sample phase followed by a choice phase. During the sample phase, rats would receive one of five different odors. Fifteen seconds later during the choice phase one of the previous odors was presented simultaneously side by side with a different odor that was based on the number of aliphatic acids that varied in the carbon chains from two- to six-carbons in length and rats were allowed to choose between the two odors. The rule to be learned in order to receive a food reward was to always choose the odor that occurred during the study phase. Odor separations of 1, 2, 3 or 4 were selected for each choice phase and represented the carbon chain difference between the study phase odor and the test phase odor. Once an animal reached a criterion of 80–90% correct across all temporal separations based on 40 trials, rats received a control, dorsal hippocampal, or ventral hippocampal lesion and were retested on the task. On postoperative trials, only the ventral hippocampal lesion group was impaired relative to both control and dorsal hippocampal groups groups. There were no effects on odor pattern separation. All groups of rats could discriminate between the odors. The data suggest that the ventral hippocampus, but not dorsal hippocampus, supports working memory for odor information.     

Effects of excitotoxic brain lesions on taste-mediated odor learning in the rat

The association learning between taste and odor is important in ingestive behavior. For a better understanding of this learning, we have developed a convenient and useful paradigm to assess the taste-mediated odor learning. In the training session, Wistar male rats drank water from two bottles in their home cages and from eight small glass dishes. In the learning session they were exposed in their home cages and also in a circular open-field apparatus to 0.005 M Na-saccharin and 0.02 M quinine hydrochloride which contained either banana or almond odors. One learning trial consisted of this pair of exposures. The preceding behavioral experiment has shown that these two odors are not aversive and are differentially perceived by rats. In the test session, the animals were put in the open-field apparatus equipped with eight dishes: four contained water with banana, and another four, with almond. Normal control rats preferred to drink water with the odor previously associated with saccharin. Stronger and more persistent preference was attained after two or three learning trials. To elucidate the brain sites responsible for this taste-mediated odor learning, the same procedure was assessed on brain-lesioned rats. Rats with lesions in the amygdala showed rapid extinction of preference to the saccharin-associated odor, whereas control rats did not. However, rats with lesions in the insular cortex showed retention of learning similar to that of the control rats. Rats with lesions in the sulcal prefrontal or cingulate cortices showed moderate disruptive effects on preference to the saccharin-associated odor. In conclusion, the odor learning established in our experimental paradigm is based on the association between the quality of odor and hedonics of taste. The amygdala may play a role in the formation, at least in the retention process, of this taste-odor association learning.     

Odor-context effects in free recall after a short retention interval: A new methodology for controlling adaptation

The present study investigated context effects of incidental odors in free recall after a short retention interval (5 min). With a short retention interval, the results are not confounded by extraneous odors or encounters with the experimental odor and possible rehearsal during a long retention interval. A short study time condition (4 s per item), predicted not to be affected by adaptation to the odor, and a long study time condition (8 s per item) were used. Additionally, we introduced a new method for recovery from adaptation, where a dissimilar odor was briefly presented at the beginning of the retention interval, and we demonstrated the effectiveness of this technique. An incidental learning paradigm was used to prevent overshadowing from confounding the results. In three experiments, undergraduates (N = 200) incidentally studied words presented one-by-one and received a free recall test. Two pairs of odors and a third odor having different semantic-differential characteristics were selected from 14 familiar odors. One of the odors was presented during encoding, and during the test, the same odor (same-context condition) or the other odor within the pair (different-context condition) was presented. Without using a recovery-from-adaptation method, a significant odor-context effect appeared in the 4-s/item condition, but not in the 8-s/item condition. Using the recovery-from-adaptation method, context effects were found for both the 8- and the 4-s/item conditions. The size of the recovered odor-context effect did not change with study time. There were no serial position effects. Implications of the present findings are discussed.     

Serial position effects in recognition memory for odors

Five experiments examined recognition memory for sequentially presented odors. Participants were presented with a sequence of odors and then had to identify an odor from the list in a test probe containing 2 odors. All experiments demonstrated enhanced recognition of odors presented at the start and end of a series, compared with those presented in the middle of the series when a 3-s retention interval between list termination and test was used. In Experiments 2 and 3, when a 30-s or 60-s retention interval was used, participants performed at slightly lower levels, although the serial position function was similar to that obtained with the 3-s retention interval. These results were noted with a 5-item (Experiments 1 and 4), 7-item (Experiment 2), 6-item (Experiment 3), and 4-item (Experiment 5) list of odors. As the number of test trials increased, recognition performance decreased, indicating a strong role for olfactory fatigue or interference in these procedures. A verbal suppression task, used in Experiments 4 and 5, had little influence on serial-position-based performance.     

Very short term recognition memory for odors

An investigation of very short term olfactory recognition memory was made with odors of low familiarity to subjects. The experimental procedure was that currently used to make qualitative similarity judgments on odors delivered in paired succession. Subjects made similarity judgments in a yes/no recognition paradigm on odors that were either identical or different. The dependence of recognition performance upon the degree of qualitative similarity was assessed by using two sets of dissimilar odor pairs: slightly dissimilar pairs (S1) and very dissimilar pairs (S2). Performance in terms of correct judgments (hits, correct rejections) was rather good for identical pairs in both sets and was nearly perfect for very dissimilar pairs with a delay of 2–300 sec, suggesting no effect of time or similarity on performance. However, for slightly dissimilar pairs, false alarms increased in number, thereby indicating a dependence of the recognition score on the qualitative distance between odors. In addition, false alarms tended to increase with the lengthening of the retention interval. It was suggested that the subjects based their responses on their capability to detect differences between odors rather than recognizing their similarities. Correct identifications were thus preserved at the cost of increasing false alarms when the discrimination task was made more difficult by closer similarity between odors (S1) or by the fading of memory traces with time. Studying the congruence between the similarity judgments and the kind of evocations associated with paired odors gives some support to the view that recognition performances had some cognitive/semantic basis.     

Neural and molecular mechanisms of microcognition in Limax

Various non-mammalian model systems are being explored in the search for mechanisms of learning and memory storage of sufficient generality to contribute to the understanding of mammalian learning mechanisms. The terrestrial mollusk Limax maximus is one such model system in which mammalian-quality learning has been documented using odors as conditioned stimuli. The Limax odor information-processing circuits incorporate several system design features also found in mammalian odor-processing circuits, such as the use of cellular and network oscillations for making odor computations and the use of nitric oxide to control network oscillations. Learning and memory formation has been localized to a particular central circuit, the procerebral lobe, in which selective gene activation occurs through odor learning. Since the isolated Limax brain can perform odor learning in vitro, the circuits and synapses causally linked to learning and memory formation are assessable for further detailed analysis.     

Implicit and explicit memories of odors

The present experiments explore whether there may be some forms of implicit memory for odors. In the first experiment, the elaborateness of olfactory encoding was varied at presentation. For (explicit) recognition memory testing we found positive effects of labeling responses to odors at encoding. Implicit memory measures (temporal and preference judgments) did not reveal reliable effects of prior odor presentation, however. The second experiment corroborated effects of levels of processing on r recognition memory. Again, perceptual or affective judgments remained insensitive for prior odor exposures. Implicit memory could only be detected with verbal measures at the testing stage (labeling accuracy or latency). These results are consistent with the proposal that odor information is represented at different levels of processing that are even with implicit memory measures only partly accessible.