Aras Petrulis

Lesions centered on the medial amygdala impair scent-marking and sex-odor recognition but spare discrimination of individual odors in female golden hamsters.

The medial amygdala (Me) has been implicated in various social behaviors that depend on chemosensory cues, but its precise role in discriminating and learning social odors is not known. Female golden hamsters (Mesocricetus auratus) received electrolytic lesions of the Me or sham surgery and were tested for their ability to (a) discriminate between odors of individual males in a habituation-discrimination task, (b) show preferences for male over female odors in a Y maze, and (c) scent-mark in response to male and female odors. All females discriminated between scents of individual males. In contrast, Me lesions eliminated female preferences for male odors in a Y maze. Females with Me lesions also showed a substantial reduction in vaginal marking and virtually no flank marking in response to odors. Thus, the Me in female hamsters is critical for differential investigation of opposite-sex odors and for scent-marking behavior but is not involved in discrimination between odors of individuals.

Effects of vomeronasal organ removal on individual odor discrimination, sex-odor preference, and scent marking by female hamsters.

Removal of the vomeronasal organ (VNX) did not eliminate the ability of female hamsters to discriminate between individual males flank gland or urine odors in a habituation/discrimination task nor did it impair preference for male odors over female odors from a distance. Vomeronasal organ removal did reduce overall levels of investigation of flank gland odor in the habituation/discrimination task. Although VNX females did not show severe impairments in the frequency of either flank or vaginal marking in response to odors, they did show an abnormal pattern of marking. VNX females, unlike shams, did not flank mark more to female odors than to male odors, nor did they vaginal mark more to male odors than to female odors. Thus, the vomeronasal organ in female hamsters appears to be important for differences in scent marking toward male and female odors, but is not essential for discrimination of individual odors or for preferences for male over female odors.

Neural mechanisms of individual and sexual recognition in Syrian hamsters (Mesocricetus auratus)

Recognizing the individual and sexual identities of conspecifics is critical for adaptive social behavior and, in most mammals this information is communicated primarily by chemosensory cues. Due to its heavy reliance on odor cues, we have used the Syrian hamster as our model species for investigating the neural regulation of social recognition. Using lesion, electrophysiological and immunocytochemical techniques, separate neural pathways underlying recognition of individual odors and guidance of sex-typical responses to opposite-sex odors have been identified in both male and female hamsters. Specifically, we have found that recognition of individual odor identity requires olfactory bulb connections to entorhinal cortex (ENT) rather than other chemoreceptive brain regions. This kind of social memory does not appear to require the hippocampus and may, instead, depend on ENT connections with piriform cortex. In contrast, sexual recognition, through either differential investigation or scent marking toward opposite-sex odors, depends on both olfactory and vomeronasal system input to the corticomedial amygdala. Preference for investigating opposite-sex odors requires primarily olfactory input to the medial amygdala (ME) whereas appropriately targeted scent marking responses require vomeronasal input to ME as well as to other structures. Within the ME, the anterior section (MEa) appears important for evaluating or classifying social odors whereas the posterodorsal region (MEpd) may be more involved in generating approach to social odors. Evidence is presented that analysis of social odors may initially be done in MEa and then communicated to MEpd, perhaps through micro-circuits that separately process male and female odors.

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 females 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.

The perirhinal–entorhinal cortex, but not the hippocampus, is critical for expression of individual recognition in the context of the Coolidge effect

The Coolidge effect is a phenomenon in which males show renewed sexual interest in a novel female following copulation to satiety with another female. In golden hamsters, this phenomenon depends on the ability to recognize conspecifics using chemosensory cues processed through the main olfactory system. Here we tested whether olfactory targets in the hippocampal system support this natural form of recognition memory. Male hamsters received ibotenic acid lesions of the perirhinal-entorhinal cortex (PR-ENT) or hippocampus (H) and were allowed to copulate to satiety with a female conspecific, then were presented with two anesthetized females, the familiar mate and an unfamiliar female that copulated with another male. Sham-operated and H-lesioned subjects preferentially investigated the novel female, indicating intact recognition of individual identity. By contrast, PR-ENT-lesioned males failed to discriminate familiar and novel females, and this deficit could not be attributed to abnormal copulatory behavior during mating. All subjects were able to detect and discriminate between female odors when presented in isolation during a habituation-discrimination test, indicating that behavioral deficits shown by PR-ENT males were not due to anosmia or a general investigatory deficit. Thus, the perirhinal-entorhinal cortex, but not the hippocampus, is critical for the recognition of familiar conspecifics in this naturalistic situation. This study reveals an essential role for the perirhinal-entorhinal cortex, but not the hippocampus, in a natural form of recognition memory within the social behavior of hamsters. The findings show a strikingly similar pattern to the effects of selective damage to the same brain regions on performance in standard recognition memory tasks by rats and monkeys. Therefore, the present data extend our understanding of the differential role of structures of the hippocampal memory system, showing continuity across species and between formal laboratory tests and the function of memory in natural social behavior.

Chemosensory and steroid-responsive regions of the medial amygdala regulate distinct aspects of opposite-sex odor preference in male Syrian hamsters.

In rodent species, such as the Syrian hamster, the expression of sexual preference requires neural integration of social chemosensory signals and steroid hormone cues. Although anatomical data suggest that separate pathways within the nervous system process these two signals, the functional significance of this separation is not well understood. Specifically, within the medial amygdala, the anterior region (MEa) receives input from the olfactory bulbs and other chemosensory areas, whereas the posterodorsal region (MEpd) contains a dense population of steroid receptors and receives less substantial chemosensory input. Consequently, the MEa may subserve a primarily discriminative function, whereas the MEpd may mediate the permissive effects of sex steroids on sexual preference. To test these hypotheses, we measured preference and attraction to female and male odors in males with lesions of either the MEa or MEpd. In Experiment 1, lesions of either region eliminated opposite‐sex odor preferences. Importantly, MEpd‐lesioned males displayed decreased attraction toward female odors, suggesting decreased sexual motivation. In contrast, MEa‐lesioned males displayed high levels of investigation of both male and female odors, suggesting an inability to categorize the relevance of the odor stimuli. In Experiment 2, we verified that both MEa‐ and MEpd‐lesioned males could discriminate between female and male odors, thereby eliminating the possibility that the observed lack of preference reflected a sensory deficit. Taken together, these results suggest that both the MEa and MEpd are critical for the expression of opposite‐sex odor preference, although they appear to mediate distinct aspects of this behavior.

Recognition of competitors by male golden hamsters

Golden hamsters, like many animals, form dominant/subordinate relationships after aggressive encounters. We examined whether behavioral responses by males that won or lost fights would differ toward familiar and unfamiliar male stimulus animals. In Experiment 1, male winners or losers of fights explored an arena containing a confined stimulus animal that was either familiar or novel and had either won or lost a fight. Compared to dominant males, losers spent less time in proximity to stimulus males and investigated them less. Losers also displayed higher levels of stretch-attend postures (indicative of risk assessment) than winners, and they showed more escape and locomotion in response to familiar winners than to unfamiliar winners, indicating recognition of the male that they had lost to. In Experiment 2, losers scent marked less to the odors of a familiar winner than to those of an unfamiliar winner. Thus, male hamsters appear to use familiarity with a former opponents odors to adaptively regulate their responses to variations in social threat.

Chemosignals and hormones in the neural control of mammalian sexual behavior

Males and females of most mammalian species depend on chemosignals to find, attract and evaluate mates and, in most cases, these appetitive sexual behaviors are strongly modulated by activational and organizational effects of sex steroids. The neural circuit underlying chemosensory-mediated pre- and peri-copulatory behavior involves the medial amygdala (MA), the bed nucleus of the stria terminalis (BNST), medial preoptic area (MPOA) and ventromedial hypothalamus (VMH), each area being subdivided into interconnected chemoreceptive and hormone-sensitive zones. For males, MA-BNST connections mediate chemoinvestigation whereas the MA-MPOA pathway regulates copulatory initiation. For females, MA-MPOA/BNST connections also control aspects of precopulatory behavior whereas MA-VMH projections control both precopulatory and copulatory behavior. Significant gaps in understanding remain, including the role of VMH in male behavior and MPOA in female appetitive behavior, the function of cortical amygdala, the underlying chemical architecture of this circuit and sex differences in hormonal and neurochemical regulation of precopulatory behavior.

A reevaluation of dimethyl disulfide as a sex attractant in golden hamsters

Dimethyl disulfide (DMDS) is present in hamster vaginal secretion and has been reported to be responsible for a sizable proportion of a male hamsters attraction to vaginal secretion. We evaluated this claim by testing two predictions that follow from its purported pheromonal role: (a) male hamsters should spend more time than females investigating DMDS; and (b) attraction to DMDS by males should be dependent on testosterone. In the first experiment, males investigated vaginal secretions more than females, but no sex difference was apparent in investigation of DMDS or a control odor. In the second experiment, gonadectomized males with testosterone implants investigated vaginal secretion more than castrates without testosterone; however, these hormone manipulations did not affect the attraction of males to DMDS or the control odor. We conclude that DMDS does not elicit sex differences in attraction and that in males the attraction to DMDS is not dependent on gonadal hormones. These results suggest that DMDS is not a sex attractant by itself nor is it a major component of an attractant mixture.

The role of the hippocampal system in social odor discrimination and scent-marking in female golden hamsters (Mesocricetus auratus).

Female golden hamsters (Mesocricetus auratus) received aspiration lesions of the parahippocampal region (PARA) or electrolytic lesions of the fimbria-fornix (FNX) and were tested for their (a) discrimination between odors of individual males in a habituation-discrimination task, (b) preference for male over female odors, and (c) scent-marking in response to conspecific odors. Both lesion groups habituated to repeated presentations of a males odor. However, only FNX females discriminated between scents of individual males, whereas PARA females did not. Neither lesion eliminated female preferences for male odors. Females with FNX lesions showed decreased levels of scent marking, but those with PARA lesions had more subtle deficits. Thus, the PARA, but not the subcortical connections of the hippocampus, is critical for discrimination of the odors of individuals.