Development of individually distinct recognition cues

Despite extensive research on the functions of kin recognition, little is known about ontogenetic changes in the cues mediating such recognition. In Belding's ground squirrels, Spermophilus beldingi, secretions from oral glands are both individually distinct and kin distinct, and function in social recognition across many contexts. Behavioral studies of recognition and kin preferences suggest that these cues may change across development, particularly around the time of weaning and emergence from natal burrows (around 25 days of age). I used an habituation-discrimination task with captive S. beldingi, presenting subjects with odors collected from a pair of pups at several ages across early development. I found that at 21 days of age, but not at 7 or 14, young produce detectable odors. Odors are not individually distinct, however, until 28 days of age, after young have emerged from their burrows and begun foraging. In addition, an individual's odor continues to develop after emergence: odors produced by an individual at 20 and 40 days of age are perceived as dissimilar, yet odors produced at 28 and 40 days are treated as similar. Developmental changes in odors provide a proximate explanation for why S. beldingi littermate preferences are not consolidated until after natal emergence, and demonstrate that conspecifics must update their recognition templates as young develop.     

Kin recognition in the sweat bee,Lasioglossum zephyrum

Recognition of kin in sweat bees is dependent upon social learning. Shortly after emergence as adults, bees learn the odors of nestmates, normally relatives, and use this knowledge to keep nonnestmate (and therefore nonkin) bees out. The odors are heritable so that once a bee learns the odors of its kin, it can recognize other kin that it has never met before. An individual guard bee does not seem to use knowledge of self as a reference. Larval learning of odors, common rearing of offspring, maternal inheritance, and inbreeding effects are not sufficient to explain the recognition of unfamiliar relatives. Individual guard bees can discriminate between close and distant relatives. Kin recognition may be a secondary or serendipitous use of odors that originally evolved for the recognition of mates and nest entrances.This work was supported by NSF Grant BNS 82-00651 (C. D. Michener, principal investigator).     

Human kin recognition by olfactory cues

T-shirts worn by individual children were correctly identified by the siblings and mothers of those children through olfactory cues alone. Furthermore, parents correctly distinguished between the odors of otherwise identical shirts worn by two of their own children. Bodily odors may therefore be salient stimuli for kin recognition among humans.     

Selective depletion of bacteria alters but does not eliminate odors of individuality in Rattus norvegicus

To determine if odors of individuality are influenced by the removal of Gram-negative or Gram-positive gut bacteria, Long-Evans rats were trained in an operant olfactometer to discriminate between the odors of two individual conspecifics and their operant responses to three different odors in randomly presented probe trials were analyzed. Significantly more responses were made to the probe odors from two known individuals than to the probe odors from known individuals with their Gram-negative bacteria eliminated (Experiment 1) or their Gram-positive bacteria eliminated (Experiment 2). Responses to the probe odors from known rats with bacterial selectively depleted did not differ significantly from responses to probe odors from unknown rats. These results support the hypothesis that the urinary odor of an individual rat is altered by the removal of specific gut bacteria. In Experiments 3 and 4, subjects made fewer errors in learning to discriminate between the odors of the familiar rats whose bacteria had been selectively depleted than between the odors of unknown rats. This "savings effect" indicates that some components of the individual urinary odors were retained after the removal of specific gut bacteria. Thus, the eliminated bacteria were not totally responsible for the odors of individuality. The outcome of Experiments 3 and 4 also indicates that conclusions regarding the recognition of odors by rats should not be made on the outcome of probe trial experiments alone.     

Ecological correlates and potential functions of kin recognition and kin association in anuran larvae

The larvae of seven species of anurans differ significantly in their abilities to discriminate between kin and nonkin. The ontogeny of kin recognition in certain species is greatly influenced by the environment in which they are reared. In other species, the rearing regime has little affect on the development of kin recognition. Larvae of some anurans develop a kin recognition system in the absence of cues from other individuals. Natural conditions of embryonic development, larval dispersal characteristics, and aggregation behavior are correlated with the kin recognition system of most anurans examined. However, these ecological characteristics are not consistent with the kin recognition systems displayed by a few species. Warning relatives, through the release of chemical signals, and enhancement of growth and development are potential functions of kin association. Intraspecific competition and cannibalism directed toward nonkin are possible functions of kin recognition.     

Individual odors of rats are discriminable independently of changes in gonadal hormone levels

Male Long-Evans hooded rats were tested for their ability to discriminate between the urine odors from individual outbred Long-Evans rats using the habituation-dishabituation method. There were discriminable differences between the urine odors of two individual intact males, castrated males, estrous/proestrous females, diestrous/metestrous females and ovariectomized females. Thus, individual outbred rats of both sexes can be discriminated on the basis of their urine odors using this technique and discrimination between individuals occurs despite changes in gonadal hormone levels. This suggests that individual recognition is independent of reproductive state and social status although these may influence the production of body odors used for individual discrimination in rats. Individual odors most likely reflect genetic differences between individuals within the outbred strain.     

Rats can discriminate between the urine odors of genetically identical mice maintained on different diets.

Male Long-Evans hooded rats were tested in a habituation-dishabituation procedure for their ability to discriminate between the urine odors of male C57BL/6J mice maintained on two different diets. There were discriminable differences between the urinary odors of two individual mice maintained on different diets. The rats did not dishabituate when presented with urine odors from two individuals on the same diet or two odor samples from the same individual. These results indicate that individual urinary odors of genetically identical mice are influenced by diet. We discuss the hypothesis that diet may act together with genetic differences, commensal bacteria, and hormonal changes to convey olfactory information used for individual recognition.     

Rats assess degree of relatedness from human odors

Despite widespread interest in the evolutionary implications of human olfactory communication, the mechanisms underlying human odor production are still poorly understood. Previous studies have demonstrated that human odor cues are related to variations in the major histocompatibility complex, but it is unclear whether odors are associated with overall genotypic variation. In this study, we investigated whether more closely related humans produce more similar odor cues. To assess objective odor qualities we tested odor similarity using rats in a habituation–discrimination paradigm. Rats were first habituated to a referent human odor and were then presented with two test odors obtained from individuals related in different degrees to the referent. Investigation times for each odor were compared. Because rats investigate novel odors longer than familiar odors, we were able to determine which test odor the rats perceived as more similar to the referent human odor. For six of ten odor donor families, rats investigated the odor of the less closely related individual significantly longer than that of the more closely related individual, and investigation durations were in the expected direction for all families. These results indicate that similarity of human odor cues is associated with degree of genetic relatedness, with more closely related humans producing more similar odor cues. This study supports the hypothesis that odor cues provide information regarding degree of relatedness and may thus affect a wide variety of human behaviors, including kin preferences, nepotism, and mate choice.     

Respiratory responses to olfactory stimuli in Parkinson's disease

There are many reports of olfactory impairment in patients with Parkinson's disease (PD) and the impairment can be observed before the appearance of typical PD symptom. Accordingly, olfactory screening tests may predict disease onset and indicates a need for early treatment before classic signs of the disease. Olfaction is dependent on inspiration, and activation of olfactory limbic areas are synchronized with the natural breathing cycle in animals and humans. Subconscious changes in respiratory pattern occur in response to odor stimulation. The use of olfactory stimuli to investigate respiratory pattern could be used to assess olfactory perception and serve as an index for olfactory limbic activation. In this study, we tested olfactory acuity in normal subjects and in patients with PD and recorded V(O2) and respiratory variables during pleasant and unpleasant odor presentation. All subjects were able to detect the odorants; however patients with PD were assigned to one of two groups, group that could recognize odors or the group with impaired odor recognition. Respiratory response toward unpleasant and pleasant odor recognition were weak in PD groups who could recognize odors than normal subject as well as emotional response to odor stimuli. PD group with impaired odor recognition showed no respiratory response toward odor stimuli. PD may experience difficulty in feeling positive emotions toward pleasant odors prior to the unpleasant odor because respiratory responses to pleasant odors may also be related to higher processes including intentional control of breathing pattern as a result of olfactory cortex processing and perceptions or emotions.     

Discrimination of odors from stressed rats by non-stressed rats

Comparison of earlier reports of rat stress odors is complicated by the many differences in experimental parameters and responses measured. To evaluate whether these stress odors provide a special signal, rats were subjected to different levels of stressful foot-shock in one half of a simple two-compartment test box whilst the other half was clean and unoccupied. The results show that whilst test subjects preferred the half containing odors from non-stressed rats, this preference was decreased by the presence of stress odors to an extent concordant with the level of stressor applied to the odor donors. There were no differences in plasma corticosterone among the odor donors indicating that this hormone is probably not the source of stress odors. Plasma corticosterone levels of the subjects were similar to each other and to the odor donors. Compared to odors from non-stressed rats, stress odors increased the activity of the subjects. The evidence strongly suggests a special signalling function for stress odors although responses to this signal are not stereotyped.     

Ground squirrel kin recognition abilities: Are there social and life-history correlates?

The degree to which related individuals exhibit cooperative, aid-giving behavior varies interspecifically among the ground-dwelling sciuridae, and the use of particular mechanisms to mediate kin recognition has been predicted to vary accordingly. Recent studies of kin recognition mechanisms in Spermophilus indicate that both mother-offspring and sibling recognition is facilitated by familiarity established during early association and that odor is the most probable cue on which discriminations are based. In three of four species, empirical evidence suggests that phenotype matching and/or recognition alleles can supplement the familiarity effects for siblings. This interspecific variation is discussed in terms of (1) differential occurrence of the contexts proposed to promote phenotype matching, (2) differential opportunities for implementing discriminations of various classes of relatives, and (3) differential selection for channeling preferential treatment toward genetic relatives. Although the observed variation appears to be consistent with 3 and perhaps 2, the assumption that the mechanisms used in recognizing particular classes of relatives are ontogenetically stable and species typical is questioned.     

Impairment of odor recognition in Parkinson's disease caused by weak activations of the orbitofrontal cortex

Olfactory dysfunction and abnormalities of olfactory brain structures are found in patients with Parkinson's disease (PD), and a number of studies have reported that olfactory dysfunction is caused by abnormalities of the central olfactory systems. We previously analyzed electroencephalograms (EEGs) and respiration simultaneously in normal subjects while testing for detection and recognition of odors. We identified changes in respiration pattern in response to odor stimuli and found inspiratory phase-locked alpha oscillations (I-alpha). The genesis of I-alpha were identified in olfactory-related areas including the entorhinal cortex, hippocampus, amygdale and orbitofrontal cortex with an EEG dipole tracing method. In the present study, we used the same protocol in PD patients and compared results of PD with those of age-matched controls. All PD patients detected odor, but 5 out of 10 showed impaired odor recognition. Changes in breathing pattern associated with emotional changes during exposure to odor stimuli were not observed in PD patients. I-alpha waveforms were not observed; however, positive waves followed by negative waves were identified approximately 100ms after inspiration onset. Dipoles of this component were localized in the entorhinal cortex for odor detection in all patients and in the entorhinal cortex and middle temporal gyrus for PD patients who could discriminate odors. Odor recognition in PD could be subserved by a different neural circuit from that of normal subjects, done through the temporal association cortex as a subsystem for recognizing the odor; however, the system may not be associated with the odor-induced emotions.     

Neural correlates of social odor recognition and the representation of individual distinctive social odors within entorhinal cortex and ventral subiculum

Recognition of individual conspecifics is important for social behavior and requires the formation of memories for individually distinctive social signals. Individual recognition is often mediated by olfactory cues in mammals, especially nocturnal rodents such as golden hamsters. In hamsters, this form of recognition requires main olfactory system input to the lateral entorhinal cortex (LEnt). Here, we tested whether neurons in LEnt and the nearby ventral subiculum (VS) would show cellular correlates of this natural form of recognition memory. Two hundred ninety single neurons were recorded from both superficial (SE) and deep layers of LEnt (DE) and VS while male hamsters investigated volatile odorants from female vaginal secretions. Many neurons encoded differences between female's odors with many discriminating between odors from different individual females but not between different odor samples from the same female. Other neurons discriminated between odor samples from one female and generalized across collections from other females. LEnt and VS neurons showed enhanced or suppressed cellular activity during investigation of previously presented odors and in response to novel odors. A majority of SE neurons decreased firing to odor repetition and increased activity to novel odors. In contrast, DE neurons often showed suppressed activity in response to novel odors. Thus, neurons in LEnt and VS of male hamsters encode information that is critical for the identification and recognition of individual females by odor cues. This study reveals cellular mechanisms in LEnt and VS that may mediate a natural form of recognition memory in hamsters. These neuronal responses were similar to those observed in rats and monkeys during performance in standard recognition memory tasks. Consequently, the present data extend our understanding of the cellular basis for recognition memory and suggest that individual recognition requires similar neural mechanisms as those employed in laboratory tests of recognition memory.     

Sister,aunt-niece,and cousin recognition by social wasps

In blind laboratory observations, gynes (potential queens) of the social waspPolistes fuscatus discriminated nestmate sisters from unrelated nonnestmate gynes but failed to discriminate between nestmate sisters and nonnestmate aunts and nieces. Gynes treat nonnestmate aunts and nieces as nestmate sisters, indicating that gynes recognize kin other than nestmates (i.e., aunts and nieces) by using genetic odors. In blind field observations, femaleP. fuscatus discriminated between nestmate sisters and nonnestmate first cousins and unrelated nonnestmates. However, females failed to discriminate between nonnestmate first cousins and unrelated nonnestmates. The results of the laboratory and field studies provide additional support for the cue similarity threshold model of recognition, which has important sociobiological implications for social wasps.This research was supported by NSF Grant BNS 86-06817.     

The capacity of humans to identify odors in mixtures

One hundred and twenty-three subjects were given the task of identifying the constituents of stimuli consisting of 1-5 odorants. The highest level of identification occurred with single odors and few subjects correctly identified the constituents of mixtures. Since the stimuli were common, dissimilar odors, the results suggest that the capacity of humans to process information about odors perceived simultaneously may be limited, or that odors in mixtures blend to form a new odor with few of the characteristics of the constituent odors.     

Physiological evidence for genetically mediated sibling recognition in mice

The kin selection theory predicts that individuals would behave differently toward one another, depending on their genetic relatedness. Kin discrimination has been demonstrated in mice from social behavior, and previous familiarity, as well as familiarity with the partner's phenotype, has been postulated to represent proximate mechanisms. It has already been demonstrated that siblings' reunion resulted in a decrease in pain sensitivity that is mediated by endogenous opioids. In this study, using a cross-transferring design, it is shown that genetic relatedness with the male partner, independently of postnatal association, is responsible for changes in nociceptive threshold. Conversely, previous association till weaning has no effect on pain sensitivity. These data suggest that endogenous opioids activity and social behavior represent indices of different processes: the recognition of related animals and the discrimination of familiar (and also usually related) subjects, respectively.     

Influence of affective and cognitive judgments on autonomic parameters during inhalation of pleasant and unpleasant odors in humans

Hedonic tone is so salient in odor perception that several authors have used odors to induce affective states. Various studies have shown that the electrophysiological and psychophysiological response patterns induced by olfactory stimuli are different for pleasant and unpleasant odors, and that these types of odor activate brain structures differentially. These results suggest that odors are first categorized according to pleasantness. The objective of the present work was to study the possible existence of an involuntary affective categorization in olfaction. Given that certain variations in the autonomic system, such as skin conductance amplitude and heart rate, are not under the voluntary control of human subjects, we used such psychophysiological methods for this investigation. Our results indicate that unpleasant odors provoke heart-rate acceleration during both a smelling task (control condition: a task in which subjects had only to inhale odors) and a pleasantness judgment, but not during a familiarity judgment. These results suggest that subjects involuntarily categorize odors by their pleasantness.     

Individual recognition after fighting by golden hamsters: a new method

Individual recognition is crucial for many aspects of social behavior and may be a specially evolved type of learning and memory. Using golden hamsters, we developed a behavioral method for the investigation of individual recognition. After a series of three brief fights, the two males were categorized as winners or losers. In Experiments 1 and 2, the loser was then tested in a Y-maze after four different intervals (30 min, 1 day, 3 days and 7 days). In Experiment 1, the familiar winner was confined in a stimulus compartment at the end of one arm of the Y, whereas no animal occupied the opposite arm. The results showed that the losers in the experimental group spent the most time in the base of the Y (in or near the start box). They also showed hesitancy to approach the winners' odors and spent less time near them than they spent in the same area when tested with no stimulus males present. In contrast, No Fight control males spent the most time near the stimulus males and did not hesitate in approaching them. In Experiment 2, losers spent less time near the odors of a familiar winner than control losers spent near unfamiliar winners, suggesting recognition of a particular winner. In Experiment 3, the losers were tested just once, 7 days after the last interaction. Again, they spent the most time in the base of the Y and avoided the arm with odors of their specific winners. These results suggest that losers learn to recognize individuals during brief interactions and remember this information for both the short term (30 min) and the long term (at least 1 week). This behavioral method will be useful for further investigation of individual recognition and the neural mechanisms underlying this kind of memory.     

Identification of single dissimilar odors is achieved by humans with a single sniff

The duration that a single odor needs to be sniffed for identification was determined for 18 humans. A hot wire anemometer and an oscilloscope were used to monitor the duration, volume and inhalation rate of sniffs. In Experiment 1 subjects used 1, 3 or 5 natural sniffs, or an unlimited number of natural sniffs to sample seven dissimilar single odors of moderate perceived intensity, and demonstrated that each odor could be identified with a single sniff. In Experiment 2 subjects demonstrated that each of the odors could be identified with the shortest sniff (0.42 sec) they could physically achieve. In Experiment 3 tests with two of the odorants at several concentrations showed that sniff duration influences identification over a narrow range of concentrations that is just above the recognition threshold. These results together with earlier data that described the optimum conditions for the detection of an odor and the perception of odor intensity, provide information that is necessary for the development of a standard olfactometer and standard methods for human olfactory measurements.     

The sources of odors from stressed rats

Recent studies [8,9] have shown that odors from stressed Norway rats act as signals to which other rats respond primarily by overall changes in activity and exploration. At present the source of these odors is unknown. In this study odors from urine, feces and the bodies of stressed rats were delivered along a runway in which the subjects had been previously trained to run for a water reward in the presence of odors from non-stressed rats. The results indicate that odors are released from the body surface and in the urine but not the feces of stressed rats.