Serial position effects in recognition memory for odors: A reexamination

Seven experiments examined recognition memory for sequentially presented odors. Following Reed (2000), participants were presented with a sequence of odors and then required to identify an odor from the sequence in a test probe comprising 2 odors. The pattern of results obtained by Reed (2000, although statistically marginal) demonstrated enhanced recognition for odors presented at the start (primacy) and end (recency) of the sequence: a result that we failed to replicate in any of the experiments reported here. Experiments 1 and 3 were designed to replicate Reed (2000), employing five-item and seven-item sequences, respectively, and each demonstrated significant recency, with evidence of primacy in Experiment 3 only. Experiment 2 replicated Experiment 1, with reduced interstimulus intervals, and produced a null effect of serial position. The ease with which the odors could be verbally labeled was manipulated in Experiments 4 and 5. Nameable odors produced a null effect of serial position (Experiment 4), and hard-to-name odors produced a pronounced recency effect (Experiment 5); nevertheless, overall rates of recognition were remarkably similar for the two experiments at around 70%. Articulatory suppression reduced recognition accuracy (Experiment 6), but recency was again present in the absence of primacy. Odor recognition performance was immune to the effects of an interleaved odor (Experiment 7), and, again, both primacy and recency effects were absent. There was no evidence of olfactory fatigue: Recognition accuracy improved across trials (Experiment 1). It is argued that the results of the experiments reported here are generally consistent with that body of work employing hard-to-name visual stimuli, where recency is obtained in the absence of primacy when the retention interval is short.     

Discriminating the stimulus elements during human odor-taste learning: a successful analytic stance does not eliminate learning

Odor "sweetness" may arise from experiencing odors and tastes together, resulting in a flavor memory that is later reaccessed by the odor. Forming a flavor memory may be impaired if the taste and odor elements are apparent during exposure, suggesting that configural processing may underpin learning. Using a new procedure, participants made actual flavor discriminations for one odor-taste pair (e.g., Taste A vs. Odor X-Taste A) and mock discriminations for another (e.g., Odor Y-Taste B vs. Odor Y-Taste B). Participants, who were successful at detecting the actual flavor discriminations, demonstrated equal amounts of learning for both odor-taste pairings. These results suggest that although a capacity to discriminate flavor into its elements may be necessary to support learning, whether participants experience a configural or elemental flavor representation may not.     

Age-related changes in odor discrimination

Odor naming and recognition memory are poorer in children than in adults. This study explored whether such differences might result from poorer discriminative ability. Experiment 1 used an oddity test of discrimination with familiar odors on 6-year-olds, 11-year-olds, and adults. Six-year-olds were significantly poorer at discrimination relative to 11-year-olds and adults, who did not differ. Experiment 2 used the same procedure but with hard-to-name visual stimuli and compared only 6-year-olds with adults (as with the remaining experiments in this study). There was no difference in performance between these groups. Experiment 3 used the same procedure as Experiment 1 but with less familiar odors. Six-year-olds were significantly poorer at discrimination than adults. In Experiment 4 the researchers controlled for verbal labeling by using an articulatory suppression task, with the same basic procedure as in Experiment 1. Six-year-old performance was the same as for Experiment 1 and significantly poorer than that of adults. Impoverished olfactory discrimination may underpin performance deficits previously observed in children. These all may result from their lesser experience with odors, relative to adults.     

Recall of odors: naming and autobiographical memories illustrate odor aftereffects

In the study phase, subjects had to encode either odors or the names there of by generating autobiographical memories, by judging the quality of the food source of the odors, or by labeling responses to odors. At the testing stage, explicit and implicit olfactory memory performance was assessed. With recognition testing, the provision of odors at study improved performance. Furthermore, recognition depended on elaborative encoding conditions with olfactory stimuli only. Implicit memory was measured by the correctness and speed of labeling responses at the testing stage. Old odors were named more correctly and faster than new ones, but only if subjects had encoded odors in the study phase. These results demonstrate that implicit memory in naming odors depends on olfactory stimulus processing and is not a purely verbal priming effect. As a further measure of implicit memory, the speed of autobiographical memory productions was assessed. We registered shorter reaction times for old versus new odors. But again, this effect of implicit memory was restricted to conditions of odor pre-experiences in the study phase. We conclude that olfactory memory is based on different types of memory traces. Implicit memory measures may prove to be useful in isolating sensory and other attributes of olfaction that seem to be interacting in making explicit memory judgments.     

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.     

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.     

Sensory and semantic factors in recognition memory for odors and graphic stimuli: elderly versus young persons

In four experiments, young (18-26 years, M = 21) and elderly (over 65 years, M = 72) people were compared for recognition memory of (a) graphic stimuli (faces of presidents and vice presidents, engineering symbols, and free forms) and (b) everyday odors. On graphic stimuli, the elderly consistently matched the young, but on odors the performance of the elderly was worse. Their poorer olfactory performance was observed after only 26 s, but became truly marked after 1 hr or more. Somewhere between 1 hr and 2 weeks, their odor performance fell to chance, but their graphic performance remained well above chance. Although the young did forget both graphic and odor materials progressively, their performance always stayed above chance over a 6-month period. Experiments 1 and 2 revealed that the elderly are less sensitive to odors than the young (with thresholds about 10-fold higher), which may explain, in part, their poorer olfactory memory performance. Knowledge that the subjects brought to the tasks by way of familiarity with and ability to name odors and faces played a positive role in recognition memory. Because of this positive role, together with the negative role played by verbal distraction, we conclude that odor recognition memory depends, perhaps heavily, on semantic processing. Impaired semantic processing may result even when odors are simply rendered desaturated, or pastel because of the weakening of olfactory sensitivity with aging.     

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.     

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.     

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.     

Recognizing odors associated with meaningful places

Thirty-two undergraduates inhaled odors while outlining episodes, set in 8 living rooms, involving either themselves or the actual inhabitants. They rated odors, rooms, and episodes on 7-point scales and were tested for odor recognition. Episodes were content analyzed, and the frequency of categories was assessed. Separate factor analyses determined relationships between rating scales and content analysis categories. Regression analysis showed greater odor recognition when participants judged the odor to fit the imagined episode but less recognition when an unpleasant odor was incongruously paired with a warm episode. Odor recognition also was greater when the narrative outlines described familiar characters figuring out the scenes. Results supported the congruity hypothesis, whereby odors become markers for meaningful scenes with which they fit.     

Recognition of common odors,pictures, and simple shapes

Recognition of common odors and simple shapes decayed in a similar manner over the course of 4 months. Recognition of complex pictures was uniformly higher than recognition of the odors and simple figures, although the distractors for these stimuli were much less similar than for the odors or simple shapes. Recognition of these common odors was the same as recognition performance on single chemicals used in previous studies. These results suggest that simple chemicals and complex familiar odors are encoded or remembered in a similar fashion, and that visual stimuli exist which are encoded in a similar manner to odors, possibly as unitary images with few features.     

Age-related changes in contextual associative learning

The hippocampus plays a critical role in processing contextual information. Although age-related changes in the hippocampus are well documented in humans, nonhuman primates, and rodents, few studies have examined contextual learning deficits in old rats. The present study investigated age-related differences in contextual associative learning in young (6 mo) and old (24 mo) rats using olfactory stimuli. Stimuli consisted of common odors mixed in sand and placed in clear plastic cups. Testing was conducted in two boxes that represented two different contexts (Context 1 and Context 2). The contexts varied based on environmental features of the box such as color (black vs. white), visual cues on the walls of the box, and flooring texture. Each rat was simultaneously presented with two cups, one filled with Odor A and one filled with Odor B in each context. In Context 1, the rat received a food reward for digging in the cup containing Odor A, but did not receive a food reward for digging in the cup containing Odor B. In Context 2, the rat was rewarded for digging in the cup containing Odor B, but did receive a reward for digging in the cup containing Odor A. Therefore, the rat learned to associate Context 1 with Odor A and Context 2 with Odor B. The rat was tested for eight days using the same odor problem throughout all days of testing. The results showed no significant difference between young and old rats on the first two days of testing; however, young rats significantly outperformed old rats on Day 3. Young rats continued to maintain superior performance compared to old rats on Days 4-8. The results suggest that aging results in functional impairments in brain regions that support memory for associations between specific cues and their respective context.     

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.     

A specific role for the human amygdala in olfactory memory

The medial temporal lobe is known to play a role in the processing of olfaction and memory. The specific contribution of the human amygdala to memory for odors has not been addressed, however. The role of this region in memory for odors was assessed in patients with unilateral amygdala damage due to temporal lobectomy (n = 20; 11 left, 9 right), one patient with selective bilateral amygdala damage, and in 20 age-matched normal controls. Fifteen odors were presented, followed 1 h later by an odor-name matching test and an odor-odor recognition test. Signal detection analyses showed that both unilateral groups were impaired in their memory for matching odors with names, these patients were not significantly impaired on odor-odor recognition. Bilateral amygdala damage resulted in severe impairment in both odor-name matching as well as in odor-odor recognition memory. Importantly, none of the patients were impaired on an auditory verbal learning task, suggesting that these findings reflect a specific impairment in olfactory memory, and not merely a more general memory deficit. Taken together, the data provide neuropsychological evidence that the human amygdala is essential for olfactory memory.     

Impaired visual and odor recognition memory span in patients with hippocampal lesions

In a recent study, rats with hippocampal lesions performed as well as did unoperated rats on an olfactory memory span task, performing ~80% correct even when the span length reached 24 odors. This finding seems potentially at odds with demonstrations that memory-impaired patients typically fail tasks in which large amounts of information must be retained. Accordingly, we have assessed recognition memory span performance for line drawings of objects, designs, and odors in amnesic patients with damage thought to be limited to the hippocampal region. The patients were impaired on all three tasks. We consider possible explanations for the difference between the findings for humans and rats, including the fact that olfactory function is particularly well-developed in rodents.     

Parallel processing in item recognition

It is shown that in Sternberg’s item recognition task Ss need not make a judgment of the absolute size or color of the test item before comparing it with memory. However, Ss do use size or color information, when possible, to reduce long reaction times for large memory loads. The results suggest that Ss are able to scan memory for form in parallel with testing for gross stimulus features, like size or color. This finding has important implications for sequential two-stage theories of attention.     

Subliminal smells can guide social preferences

It is widely accepted that unconscious processes can modulate judgments and behavior, but do such influences affect one's daily interactions with other people? Given that olfactory information has relatively direct access to cortical and subcortical emotional circuits, we tested whether the affective content of subliminal odors alters social preferences. Participants rated the likeability of neutral faces after smelling pleasant, neutral, or unpleasant odors delivered below detection thresholds. Odor affect significantly shifted likeability ratings only for those participants lacking conscious awareness of the smells, as verified by chance-level trial-by-trial performance on an odor-detection task. Across participants, the magnitude of this priming effect decreased as sensitivity for odor detection increased. In contrast, heart rate responses tracked odor valence independently of odor awareness. These results indicate that social preferences are subject to influences from odors that escape awareness, whereas the availability of conscious odor information may disrupt such effects.     

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.     

Familiarity,Cued and Free Odor Identification and Their Association with Cognitive Functioning in Middle Aged and Older Adults

ABSTRACT

The aim of the present study was to examine the association between familiarity of odors, cued and free odor identification performance and cognitive function in elderly adults. It was further investigated how age affects performance on the various odor tasks. A third aim was to investigate the role of familiarity in explaining performance on the free identification task. One hundred and thirty-six participants (aged 45–79 years) with normal olfactory sensitivity were assessed with the Scandinavian Odor Identification Test (SOIT) and standardized tests of cognitive function. Familiarity did not correlate with any measure of cognitive function, while verbal identification performance was associated with several cognitive measures, although correlations were modest. In this sample, free odor identification was affected by increasing age to a marginally larger extent than cued identification performance and familiarity ratings. The results suggest that the different olfactory tasks involve different levels of cognitive processing.