Role of the main olfactory system in recognition between individual spiny mice

Physiology & Behavior. Vol. 42, pp. 217-222. Copyright ~'PergamonPress plc, 1988. Printedin the U.S.A.

0031-9384/88$3.00 + .00

Role of the Main Olfactory System in Recognition Between Individual Spiny Mice J O H N A. M A T O C H I K 2

John F. K e n n e d y Research Center and D e p a r t m e n t o f Psychology and H u m a n D e v e l o p m e n t Vanderbilt University, Nashville, TAr 37203 R e c e i v e d 12 A u g u s t 1986 MATOCHIK, J. A. Role of the main oljhetoo, system in recognition between individual spiny mice. PHYSIOL BEHAV 42(3) 217-222, 1988.--Recognition between spiny mice requires a period of exposure to learn the olfactory cues of individual conspecifics that can serve as recognition signatures in subsequent discrimination. Animals received nasal irrigations of zinc sulfate to disrupt sensory input to the main olfactory system (MOS) either prior to the 9-day exposure period (Experiment 1) or immediately after the exposure period (Experiment 2). Animals rendered anosmic by zinc sulfate did not show evidence of recognition as defined by huddling preferences. In contrast, animals who received irrigations of saline were able to preferentially huddle with their cagemate who they had been housed with during the exposure period. The results suggest that the MOS is necessary in mediating behavioral discrimination between conspecifics. Individual recognition Olfaction Spiny mouse (Acomys cahirinus)

Social behavior

Chemical communication

THE evidence that the main olfactory (MOS) and vomeronasal (VS) systems have nearly non-overlapping neural projections has led researchers to suggest different behavioral functions for these two chemosensory systems [ l l , 30, 32, 36]. Recently, Johnston [10--12] has proposed that the MOS may be involved in the recognition of, or discrimination between, individual conspecifics or between kin and non-kin. The question addressed in the present paper concerns the role of the MOS in the mediation of recognition between individual spiny mice. The MOS may be particularly suited for social discriminations between animals. According to Johnston [11,12], learned responses to odors may be mediated by the MOS. Individual experience with an odor may be necessary to establish information value to the animal. In contrast, the VS or accessory olfactory system appears important in the facilitation of relatively inflexible, preprogrammed responses to specific chemical signals. The elicitations of LH and testosterone surges in male mice exposed to female odors is an example of a response mediated by the VS that does not seem to be dependent on experience with a particular chemical signal [37]. The MOS has also been proposed as a general molecular analyser [14] involved in analysis of complex chemical signals that may provide differential information depending on the ratios of various odor components. Such fine discriminations between complex odors may be an important prerequisite in the discrimination between individuals [3, 6, 7]. Genetic [13, 25, 39], metabolic

[2,19], and environmental [5,22] factors have been implicated in the production of odors which are sufficiently unique to convey individual identity. The spiny mouse (Acomys cahirinus) has provided a useful model to investigate the mechanisms of recognition. Several studies, including the use of cross-fostering designs, have shown that recognition of siblings or littermates develops as a result of exposure learning in the absence of an inborn ability to recognize biological siblings [24, 27-29]. Spiny mice appear to be attracted to their littermates through a process that seems to be a modifiable attraction to odors that the animals were exposed to, rather than a form of imprinting [21, 23, 25, 29]. Thus, recognition requires a period of exposure to learn the olfactory cues necessary for individual discrimination and these cues are probably complex mixtures of odors from different sources (e.g., variations in diet [5, 15, 22]). It is a reasonable hypothesis, according to the ideas presented above [l 1], that recognition between individual spiny mice is mediated by the MOS. GENERAL METHOD

Subjects The spiny mouse (A. cahirinus) is a murid rodent indigenous to the Near East. Females of the species give birth to precocial offspring; within a few hours after birth, pups are capable of independent locomotion and sensory modalities are functional. Mice were maintained in Plexiglas breeding

~Supported in part by NICHD grant HD-15051. ZRequests for reprints should be addressed to John A. Matochik, NPI 58-258, UCLA School of Medicine, Los Angeles, CA 90024.

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TABLE 1 OBSERVED FREQUENCIES OF PAIRINGS BY FAMILIAR AND UNFAMILIARANIMALS IN THE ZINC SULFATE (ZS) AND SALINE (SC) CONDITIONS Familiar Pairs

TABLE 2 OBSERVED FREQUENCIES OF PAIRINGSBY FAMILIAR AND UNFAMILIARANIMALS IN THE ZINC SULFATE (ZS) AND SALINE (SC) CONDITIONS IN EXPERIMENT 2

Unfamiliar Pairs

Familiar Pairs

ZS Condition Corrected Mean Standard Error Uncorrected Range

15.9 6.8 0-39

Corrected Mean Standard Error Uncorrected Range

207.7 8.4 114-168

Unfamiliar Pairs

ZS Condition 15.5 4.8 0-45

Corrected Mean Standard Error Uncorrected Range

28~5 9.6 0-64

0.2 0.2 0-3

Corrected Mean Standard Error Uncorrected Range

186.6 12.6 80-162

SC Condition

! t.0 4.2 0-54

S(I Condition 0.4 0.4 0-54

Results of Wilcoxon matched-pairs signed-ranks tests comparing corrected scores of familiar vs. unfamiliar pairings: For the ZS condition, Z=0.15, n (minus 1 tie)=9, NS. For the SC condition, Z=2.80, n= 10, p =0.005.

Results of Wilcoxon matched-pairs signed-ranks tests comparing corrected scores of familiar vs. unfamiliar pairings: For the ZS condition, Z---1.73, n= 10; NS. For the SC condition, Z=2.80, n=10, p =0.005.

cages on sugar cane waste bedding where adult pairs are housed with offspring until weaning. Laboratory illumination cycle was 1 3 L : l l D with lights on at 0700. Subjects were between 18-22 days postpartum (day of birth = day 1) at the beginning of the experiments. The age range was chosen because pups exhibit definite social preferences with whom they will huddle after 16 days; positive responding occurs almost exclusively toward familiar animals [26,28]. In addition, all animals tested together were of the same sex to control for sex-specific traits aiding recognition. Huddling preferences in spiny mice, however, have been shown in several experiments to be independent of sex [4, 25, 29].

limit of 15 min). If no animal in the test group found the apple, the group was assigned a latency score of 900 sec. Although the animals in a test group were not evaluated individually for evidence of anosmia, simultaneous testing entailed minimal disruption or handling of the animals prior to the test and has b e e n found t o differentiate b e t w e e n olfactory-impaired and control groups [125,29].

Procedure Each test group consisted of four animals from different litters who were unfamiliar at the start of the experiments. Animals received nasal irrigations of zinc sulfate (ZnSO4) to disrupt sensory input to MOS either prior to the 9-day exposure period (Experiment 1) or immediately after the exposure period (Experiment 2). The four animals were placed into two contact cages (18×50× 18 cm), two animals to a cage. Each pair shared the cage for nine days. A t the end of the 9-day exposure period. on day 10, the four test animals were placed into an observation terrarium (25 x 50x 31 cm). Behavior observations did not begin until 60 min later to allow the animals to become familiar with the surroundings. Observations lasted for five days with six 5-rain observation periods per day with a minimum of 30 min between successive periods. At the beginning of each 5-rain period and at the end of each min. the identities of all animals physically touching were recorded. Thus, there were six observations for each 5-min period and 36 total for each day. All observations were carried out between 0800 and 1600 hr during the light phase of the animals' light-dark cycle. At the end of the last day of testing, an independent evaluation o f olfactory impairment was conducted. Two pieces of fresh apple were buried under the bedding of the observation cage and the latency of the first animal to uncover a piece of apple was recorded (with a maximum time

Dependent Variable and Data Analvsi~s As in previous studies of recognition in spiny mice. dyadic huddling was used as a measure of social preference. Huddling was defined as body contact excluding touching of tails or vibrassae. Huddling, common in laboratorymaintained rodents [1, 26, 35], is a high baseline behavior against which manipulations can be easily assessed. The frequency of pairings by familiar (two animals who shared contact cage) and unfamiliar (animals who did not share contact cage) animals were recorded during the 5-day test period. Since huddling scores could not be considered independent because pairing by two animals would limit the remaining animals with whom they could interact, only one instance of pairing (familiar or unfamiliar) per observation point was entered into data analysis. The units o f measurement were the frequencies of pairings for each group of four animals l maximum possible s c o r e = 180) rather than scores for individual animals. Because pairings by unfamiliar animals could result from twice as many combinations o f two animals in the observation cage as familiar pairings, the expected ratio of unfamiliar to familiar pairings is 2:1 within each test group. To correct for the expected 2:1 bias, frequency of pairings by familiar animals was multiplied by a factor of 1.5 and unfamiliar pairings by 0.75. The frequency o f all four animals (three animal huddles were not included in analysis) in an observation cage huddled together was also recorded and no correction of scores was necessary for these data. Data are presented as the mean_+SEM. Results with a probability of <0.05 using twotailed nonparametrie tests were considered statistically significant,

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,

j

FIG. 1. Coronal section through the bilateral vomeronasal organs of a spiny mouse irrigated with a 5% solution of ZnSO4 2 days prior to sacrifice.

Zinc SulJ~lte Treatment The animals were anesthetized with ether and placed on their backs in an inclined position, head down, at a 45 degree angle. Approximately 0.02-0.03 ml of 5% ZnSO4 in 0.~% saline was introduced into the nasal cavity via the external nares with a blunted 26 gauge syringe needle. Animals in the control condition were given nasal irrigations of 0 . ~ saline.

Histology Since several studies in a number of species have demonstrated disruption of the MOS and sparing of the vomeronasal organ by ZnSO4 irrigations [9, 16, 18, 33, 34, 36], it was decided to run a pilot group of five animals for analysis of treatment procedure. Animals were perfused through the left ventricle with 0.9% saline followed by 10% formalin. The craniums were decalcified and the brains embedded in an egg-gel matrix for sectioning on a freezing microtome (see [36]). Coronal sections of the nasal cavity (containing the vomeronasal organs) were cut at 80 /zm and stained with cresyl violet. EXPERIMENT

l

Unfamiliar spiny mice who are housed together for nine days subsequently will display evidence of recognition by huddling preferentially with one another [24]. The 9-day exposure period presumably enables the animals to learn or become familiar with the recognition signatures of their

cagemates and allows for later behavioral discrimination. To evaluate the role of the MOS in the recognition process the sensory input to the MOS was disrupted prior to the animals being placed into contact cages. Consequently, during both the exposure and test periods, the animals were without functional use of the MOS.

Method Ten test groups were given ZnSO4 irrigations (ZS) and l0 other groups given saline irrigations (SC). After zinc sulfate treatment, animals were allowed to recover from the effects of anesthesia and then placed into contact cages. An additional ZnSO4 treatment was given on day 8 of the exposure period to ensure that input to the MOS would be disrupted during both the exposure and test periods. Animals in the SC condition were given saline irrigations also on day 8 of the exposure period.

Results The corrected frequencies of pairings by familiar and unfamiliar animals for the ZS and SC conditions are presented in Table 1. Animals rendered anosmic by ZnSO4 did not differ in their frequency of familiar vs. unfamiliar pairings while control animals huddled almost exclusively with their cagemates. It is apparent that discrimination between familiar and unfamiliar animals had broken down in the ZS groups.

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Additional statistical analysis comparing data across the two treatment conditions further characterize the impaired discrimination of animals in the ZS condition. Saline-treated control animals had significantly more recorded instances of familiar (or correc0 pairings than animals in the ZS condition (Mann-Whitney U-test, Z = - 3 . 7 8 , p=0.0003). Rather than staying in pairs. ZS animals tended to huddle into heterogenous groups containing all four animals in the observation cage (66.0-+ 16.7) while animals in the SC condition did not have any recorded instances of this kind of grouping. The results of the olfactory impairment test indicated that animals in the ZS condition took longer than SC animals to find the buried apples (Mann-Whitney U-test, Z = - 3 . 2 7 , p =0.001). Latencies to locating the apples were 630.0-+ 110.7 sec for the ZS condition and 121.8-+37.0 sec for the SC condition. Five out of the 10 ZS groups did not find the apples in the 15 minute test period. The results of histology on pilot animals to determine the effectiveness of ZnSO4 treatment showed degeneration of the olfactory epithelium in all animals. N o damage was observed to the vomeronasal organs after administration of ZnSO4 (Fig. 1). EXPERIMENT 2 In the previous experiment, it was found that disruption of the MOS impaired the animal's ability to respond discriminately toward conspecifics with which it has been housed. However. this experiment did not separate the initial familiarization process from the later recognition of a familiar conspecific. What would happen if the animals had functional use of the MOS during the exposure period but were without use of this olfactory system during the actual discrimination phase? Method

Animals were assigned to contact cages for the 9-day exposure period with no additional manipulation until day 10 when they were given ZnSO4 or saline irrigations and directly placed in observation cages. Ten ZnSO4 (ZS) and saline Control (SC) groups were run Results

The corrected frequencies of pairings by familiar and unfamiliar animals for the ZS and SC conditions are presented in Table 2. Animals made anosmic by ZnSO4 did not differ in their frequency of familiar vs. unfamiliar pairings while control animals huddled almost exclusively with their familiar cagemates. Additional analyses comparing data across the two treatment conditions further demonstrate the impaired discriminatory abilities of animals in the ZS condition. Saline-treated animals had significantly more observed instances of familiar pairings than animals in the ZS condition (Mann-Whitney U-test, Z = - 3 . 7 8 , p=0.003). Animals in the ZS condition had more instances of four-animal huddles than SC animals (Mann-Whitney U-test, Z=2.48, p=0.02). Frequencies of all four animals huddled together were 68.9-+22.7 for the ZS condition and 0.2-+0.2 for the SC condition. The results of the olfactory impairment test indicated that animals in the ZS condition took significantly longer than SC animals to locate the buried apples (Mann-Whitney U-tests, Z = - 3.81, p = 0.0001). Latencies until finding the apples were 794.0-+52.5 sec for the ZS condition and 121.2+-I3.9 sec for the SC condition. Five out of the 10 ZS groups did not find the apples during the 15 minute test period whereas all 10 groups m the SC condition successfully found the apple.

DISCUSSION The role o f the main olfactory system in the mediation of individual recognition in spiny mice was investigated in the present series of experiments. The results provide evidence that the MOS is necessary in the behavioral discrimination between conspecifics. Unpublished observations suggest that spiny mice with vomeronasal nerve cuts were correctly able to discriminate among conspecifics in our huddling preference paradigm (see [17]). However. since histology was not available for all animals tested, these observations should be viewed as tentative. The importance of the MOS in the process of individual discrimination is suggested by the results of Experiment 1. Animals rendered anosmic by ZnSO4 irrigations before being placed in contact cages were unable to preferentially huddle with their assigned cagemate and tended to huddle indiscriminately with both familiar and unfamiliar conspecifics. Control animals given saline irrigations huddled almost exclusively with their familiar cagemate. Rather than huddling in familiar pairs, ZS animals tended to form heterogenous groups comprising all four animals in the observation cage. The results of Experiment 1 indicate that the MOS is involved in the recognition process but this experiment did not differentiate between zinc sulfate effects on the initial familiarization (or learning) process from the discrimination phase. Experiment 2 was designed to evaluate the effect of disruption of the sensory input to the MOS on discrimination after the animals had the necessary exposure to learn the recognition signature o f their cagemates. Animals treated with ZnSO4 did not differ in their frequency of familiar vs. unfamiliar pairings while control animals had few instances of unfamiliar or incorrect pairings. Four-animal huddles were frequent in the ZS test groups bul rarely observed in control animals, The findings of Experiment 2 suggest that the results o f Experiment 1 could be explained b y the contribution of the MOS to the discrimination phase. The role of the MOS in the initial familiarization process was not evaluated since an experimental group lacking the MOS only during the exposure period was not run due to the variable nature of recovery from anosmia with zinc sulfate and the difficulty of matching periods of anosmia with conspecific exposure. One important difference between animals treated with ZnSO4 and the saline-treated animals is the tendency of ZS animals to huddle indiscriminately into groups containing all animals in the observation cage. The higher incidence of four-animal huddles among the ZS treatment groups in Experiments 1 and 2 strongly suggests that discrimination between animals had broken down. By comparison, animals treated with saline had very few observed instances of fouranimal huddles preferring instead to huddle with their familiar cagemate. This finding is in agreement with previous studies in which ZnSO4-treated mice had more instances of four-animal huddles than saline-treated control animals [25,29]. Unable to make consistent pair preferences, the ZS animals apparently tended to form into heterogenous groups making no discriminations between animals in the observation cage. The results of the buried apple test indicated that ZnSO4treated animals in Experiments 1 and 2 were considerably slower than animals in the control conditions in locating a food source containing volatile odor cues. F o o d finding, a function of the MOS [8,38], was severely affected in animals in the ZS condition. Histological evidence from pilot animals

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indicated degeneration of the olfactory epithelieum with sparing of the vomeronasal organs. Presumedly, the use of ether as an anesthetic increases secretions in and around the opening to the vomeronasal duct and thus protects the neural receptors from the damaging effects of ZnSO4 [18]. Since animals in the present studies were not histologically evaluated, it is possible that the vomeronasal organs may have been partially damaged. However, the results of the olfactory impairment test combined with the limited histological evidence suggests that animals in the ZS condition were significantly impaired in responding to olfactory cues. The previous study presents support for Johnston's [11] proposal that social discrimination between individual animals would be subserved by the MOS. The only study to directly compare the MOS and VS in the mediation of individual recognition used hamsters in a Coolidge effect paradigm [12]. In this study, discrimination of chemical cues by the MOS was necessary for recognition of novel females by sexually satiate males. That social discriminations are an important function of the MOS is demonstrated in a study by

Murphy [20]. Male Syrian hamsters displayed sexual preferences (e.g., body investigation, mounting) toward female conspecifics rather than Turkish hamsters who are genetically quite similar and only recently taxonomically classified as a separate species. Vomeronasal nerve cuts had no effect on the discrimination of mating partners implying MOS function as contributing to reproductive isolation in this species. The results of the present studies provide evidence that recognition between individual spiny mice can be mediated by the MOS. If the MOS mediated individual recognition in spiny mice, it could potentially allow for a more complex social organization in this species. The presumed greater flexibility of the MOS relative to the VS in mediating recognition based on learned association with conspecific odors could function in the formation of social ranks and differential treatment of individuals where discrimination of important conspecifics would change over time. Animals could, for instance, engage in reciprocal altruism with close kin as well as unrelated conspecifics [25,31].

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