Different importance of the volatile and non-volatile fractions of an olfactory signature for individual social recognition in rats versus mice and short-term versus long-term memory

doi:10.1016/j.nlm.2010.09.013

Neurobiology of Learning and Memory

Volume 94, Issue 4, November 2010, Pages 568-575

https://doi.org/10.1016/j.nlm.2010.09.013 Get rights and content

Abstract

When tested in the olfactory cued social recognition/discrimination test, rats and mice differ in their retention of a recognition memory for a previously encountered conspecific juvenile: Rats are able to recognize a given juvenile for approximately 45 min only whereas mice show not only short-term, but also long-term recognition memory (⩾24 h). Here we modified the social recognition/social discrimination procedure to investigate the neurobiological mechanism(s) underlying the species differences. We presented a conspecific juvenile repeatedly to the experimental subjects and monitored the investigation duration as a measure for recognition. Presentation of only the volatile fraction of the juvenile olfactory signature was sufficient for both short- and long-term recognition in mice but not rats. Applying additional volatile, mono-molecular odours to the “to be recognized” juveniles failed to affect short-term memory in both species, but interfered with long-term recognition in mice. Finally immunocytochemical analysis of c-Fos as a marker for cellular activation, revealed that juvenile exposure stimulated areas involved in the processing of olfactory signals in both the main and the accessory olfactory bulb in mice. In rats, we measured an increased c-Fos synthesis almost exclusively in cells of the accessory olfactory bulb. Our data suggest that the species difference in the retention of social recognition memory is based on differences in the processing of the volatile versus non-volatile fraction of the individuals’ olfactory signature. The non-volatile fraction is sufficient for retaining a short-term social memory only. Long-term social memory – as observed in mice – requires a processing of both the volatile and non-volatile fractions of the olfactory signature.

Research highlights

► Mice and rats differ in their social memory performance. ► Mice recognize conspecifics by their volatile and non-volatile odours. ► This results in long-term recognition memory. ► Rats rely on the conspecifics’ non-volatile odours. ► This results in short-term recognition memory only.

Introduction

Complex social behavioural patterns in rodent populations, including control of dominant aggression and rank order, require individual recognition. Rats and mice are known to belong to those species which developed such complex social behavioural patterns and therefore are able to form a social recognition memory.

It is well documented that social recognition memory in rodents relies on the acquisition and processing of an individual’s olfactory signature, which is composed of volatile and non-volatile compounds (Carr et al., 1976, Matochik, 1988, Popik et al., 1991, Sawyer et al., 1984) by two segregated neuronal pathways. The main olfactory system (MOS) is specialised in the processing of volatile stimuli. Volatile odours are detected by sensory neurons in the main olfactory epithelium that transfer the information to the main olfactory bulb (MOB) as the relay station to higher brain areas including hippocampus and primary olfactory cortex. The second pathway comprises the accessory olfactory system (AOS) that processes the information linked to non-volatile, predominantly pheromonal signals (Dulac & Torello, 2003). Such stimuli are collected by direct contact for instance to body fluids (Luo et al., 2003, Wysocki et al., 1985) and predominantly detected via the vomeronasal organ (VNO). Sensory neurons of the VNO project to interneurons in the accessory olfactory bulb (AOB), which in turn signal via the amygdala and bed nucleus of stria terminalis to the hypothalamus to finally elicit neuroendocrine and behavioural effects (Li et al., 1990, Simerly, 1990, Swanson and Petrovich, 1998).

Under laboratory conditions, social recognition memory in rats and mice is investigated by using the olfactory recognition/discrimination test (Engelmann et al., 1995, Thor and Holloway, 1982). This test takes advantage of the innate drive of rodents to investigate unfamiliar individuals more than familiar ones. In a typical experimental set up, an adult experimental subject acquires the olfactory signature of a juvenile conspecific during an initial encounter called sampling. After a defined exposure interval, the adult is exposed to the same juvenile together with an unfamiliar juvenile during a second encounter (choice). A significantly longer duration of social investigatory behaviour towards the unfamiliar juvenile during choice is considered to reflect recognition of the originally encountered animal.

As demonstrated by numerous publications, the social recognition/discrimination test and its modifications have been successfully applied in various laboratories to study social recognition memory in both mice and rats (Engelmann et al., 1995, Kogan et al., 2000, Popik et al., 1991, Richter et al., 2005, Squires et al., 2006). Interestingly a critical review of this literature reveals a remarkable species difference: Whereas male mice show long-term recognition memory up to 7 days, male rats are able to form short-term recognition memory for newly encountered conspecifics for approx. 45 min only. Group-housing has been reported to be of critical importance for the formation of long-term recognition memory in mice (Kogan et al., 2000), but did not improve the performance of rats in this social recognition test (Squires et al., 2006).

The present study was designed to obtain further insight into the neurobiological mechanism(s) underlying the difference between rats and mice in the retention of social memory. It is known that long-term, but not short-term, social memory critically depends upon hippocampal functioning (Kogan et al., 2000, Squires et al., 2006), thereby suggesting a different importance of the MOS versus AOS for memory performance. Direct investigation of the stimulus animals during sampling and choice allows the acquisition of both the volatile and non-volatile components of the olfactory signature. Thus the observed differences in the social memory retention between rats and mice may be caused by species-specific processing of these two components. To test this hypothesis, we modified the social discrimination test and investigated the impact on juvenile recognition in rats and mice: First animals presented as social stimuli were additionally scented with a volatile odour. Second we allowed the experimental subjects to acquire during sampling and/or choice either the full olfactory signature or its volatile fraction only. We performed c-Fos immunocytochemistry in both the AOB and MOB after the presentation of the full olfactory signature or its volatile fraction only to detect possible correlates of cellular activity that might provide further insight into the involvement of the AOS and the MOS in the processing of the different components of the olfactory signature in rats versus mice.

Section snippets

Animals

Adult male C57BL/6JOlaHsd mice and adult male Wistar rats were purchased from Harlan-Winkelmann and used for experiments at an age of 9–16 weeks. The experimental subjects were kept in groups of five under standard laboratory conditions with a 12 h:12 h light–dark cycle (lights on at 6:00 am) and provided with food and water ad libitum. Juvenile C57BL/6JOlaHsd mice and Wistar rats of both sexes (25–35 days old) were used as olfactory stimuli. Previous extensive studies in our laboratory have

Species-specific effects of different exposure intervals on recognition memory

As shown in Fig. 1B, mice were able to discriminate between both juveniles during all exposure intervals. In contrast, rats recognized the already encountered J1 at an exposure interval of 0.5 h only. At exposure intervals of 2 and 24 h rats failed to discriminate between J1 and J2 (Fig. 1C).

Scented juveniles

As shown in Fig. 3A (left panel) mice were able to recognize J1 even if it was differently scented during choice than during sampling at an exposure interval of 0.5 h. However, the normally seen long-term

Discussion

The well documented difference in the retention of social memory cued by olfactory signals between rats and mice opened the question for the possible underlying neuronal mechanism(s). As tested using different modifications of the social discrimination procedure, our results seemingly not only provide an explanation for this species difference, but also suggest a different importance of the volatile versus non-volatile fraction of the rodent’s olfactory signature for short-term versus long-term

Conflict of interest

None declared.

Acknowledgements

The authors thank Rita Murau and Andrea Mohrmann für expert technical assistance. Supported by DFG.

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Different importance of the volatile and non-volatile fractions of an olfactory signature for individual social recognition in rats versus mice and short-term versus long-term memory

Abstract

Research highlights

Introduction

Section snippets

Animals

Species-specific effects of different exposure intervals on recognition memory

Scented juveniles

Discussion

Conflict of interest

Acknowledgements

Hormones and Behavior

Brain Research

Neurobiology of Learning and Memory

Physiology and Behavior

Progress in Neurobiology

Behavioural Brain Research

Molecular and Cellular Neurosciences

Neuroscience

Neuroscience

Physiology and Behavior

Physiology and Behavior

Hormones and Behavior

Physiology and Behavior

Physiology and Behavior

Trends in Neurosciences

Neurobiology of Learning and Memory

Trends in Neurosciences

Ontogenetic changes in odor sensitivity, olfactory receptor area and olfactory receptor density in the rat

Chemical Senses

Performance of mice in an automated olfactometer: Odor detection, discrimination and odor memory

Chemical Senses

Long-term social memory in the laboratory rat (Rattus norvegicus)

Animal Welfare

Olfactory recognition of conspecifics by domestic Norway rats

Journal of Comparative and Physiological Psychology