Robert Elliott Johnston - US grants

The understanding of processes involved in species, sex, individual and kin recognition are of fundamental importance to virtually all multicellular animals. Among many mammals, chemosensory signals provide one of the most important channels of communication for such recognition. Dr. Johnston will examine the ways in which animals recognize others of their species by chemical cues and investigate the neural mechanisms underlying such recognition. His research involves the development of innovative habituation paradigms to measure individual discrimination and individual recognition. He will utilize the behavioral information to determine the roles that the two main olfactory pathways, the main olfactory system and the vomeronasal system, play in mediating the recognition processes. Not only will this multidisciplinary approach provide information towards our understanding of animal communication systems but will contribute to our understanding of (1) recognition mechanisms in general, (2) the functions of the sense of olfaction, (3) the organization and functions of the neural pathways of the olfactory system, and (4) the processing of olfactory information in different brain regions. The understanding and treatment of clinical disorders associated with taste and olfactory dysfunctions in humans can only benefit from advances in basic knowledge of animal olfaction and chemical communication research.

The goals of this research are to increase our understanding of the mechanisms of social recognition and perception at the behavioral level of analysis. Since this particular project involves communication by odors, another goal is to increase our understanding of the functions and mechanisms of the olfactory system. Recent biological theory has emphasized the importance of the individual organism in the process of evolution, yet we still know very little about the mechanisms of individual recognition and species similarities and differences in the perception of individuals and knowledge of individuals. This project will investigate some surprising new phenomena that suggest that animals have specialized perceptual and/or cognitive strategies to discover a wide variety of information about other individuals by investigation of the complex arrays of scents that are left behind in the environment. These discoveries suggest entirely new processes of olfactory perception and consequently of neural mechanisms underlying these processes. Furthermore, characterization of these strategies should provide insight into the features or aspects of individuals that have proven to be important for animals to know about, and therefore that have been important in the evolution of their behavior and of modules in the brain to accomplish this kind of social knowledge. These experiments have importance for at least three domains of science, and may well have some practical applications in the future. First, they will be important for our understanding of animal behavior, in particular about how scent is used to regulate social interactions, but more generally about social recognition, territoriality, dominant subordinate interactions, mate choice, and competition for mates and other resources. The results may have practical implications for how to maintain healthy animals in captivity in zoos, labs, and as pets, and it could well be important in wildlife management in these times of shrinking reserves for wildlife. Second, it is important for understanding higher-order, cognitive processes in the sense of smell. Third, the results should contribute to our knowledge and understanding of social recognition processes in humans and other species, processes that are gaining increasing attention in areas such as cognitive neuroscience, artificial intelligence, machine and/or computer recognition processes, and security and law enforcement (e.g., evidence from dogs or other animals about the identity of the perpetrator of a crime).

The goal of this proposal is to understand the neural mechanisms of social recognition and memory. This information will lead to a more thorough understanding of the brain, and especially of higher-order sensory processes associated with the olfactory and vomeronasal senses. In addition, the research will provide a new, unique perspective on the functional neuroanatomy of memory by investigating the role of various brain loci in social memory. Understanding of the brain, and especially of social recognition and memory processes, is relevant to the understanding of many types of human disabilities due to stroke or head injury, and also to understanding the deficits caused by a variety of degenerative diseases, including Alzheimer's disease and Korsakoff's syndrome. The specific aims of the study are to use the extensive knowledge obtained about social communication in hamsters as a model system to investigate the neural mechanisms of individual recognition by odors. Three approaches will be employed. First the roles of three different brain systems in individual recognition and memory will be studied by use of lesions. The effects of stereotaxic lesions, placed in (1) thalamus and neocortex, (2) entorhinal cortex and hippocampus, or (3) various parts of the amygdala, will be evaluated using a battery of behavioral tests. Second, cells that are activated during individual discrimination will be studied by histological methods, initially with a stains for the immediate early gene c-fos. Third, the roles of the vomeronasal and olfactory sensory systems will be investigated using lesions of the peripheral receptors. The abilities of animals to discriminate and recognize individuals after such lesions will be evaluated, thus demonstrating the roles of these two sensory systems in providing the initial input of individually distinctive information. These converging lines of evidence should provide a basis for further, finer-grained anatomical and neurophysiological investigations of social recognition and should provide a compelling addition to other approaches to the neural basis of learning and memory.

9724007 Johnston This proposal concerns mechanisms of olfactory perception and communication, particularly with regard to competition between individuals by scent marking. Most mammals communicate their individual identity and other information by scent marking, and many species that scent mark also scent over-mark (deposit their scent in the same location that other individuals have deposited scent). It has recently been discovered that, in at least two species of rodents, individuals can determine which of two individuals' scents is on top in an over-mark, regardless of whether the two scents are completely or only partially overlapping. Animals can thus determine which animal has marked most recently. The data suggest: (1) that the animals have a perceptual/cognitive strategy to determine which scent was deposited most recently; and (2) that they have some previously unsuspected sensory mechanisms to accomplish this. In this research, behavioral experiments will be carried out to investigate the functions of these extraordinary abilities, particularly with regard to the related hypotheses that (a) individuals engage in scent marking competitions in order to maintain their scent as the most recent scent in an area and (b) that other individuals evaluate scent over- marks as one means of assessing the quality of potential mates. Specifically, females may prefer males that are persistent at over-marking because this is a measure of male vigor and quality. These experiments will involve both typical laboratory tests using habituation-discrimination methods and other experiments using semi-natural laboratory enclosures to approximate the complexity of natural situations. In the specific context of the sense of smell and its role in animal behavior, this research will clarify the significance of a newly discovered ability to analyze spatial arrays of individual scents and determine which scent is on top (that is, to perceive "depth" or recen cy in arrays of individual odors). This perceptual ability probably occurs in many species and is potentially important in a wide range of situations. Our research aims to determine why such abilities have evolved, and to investigate the specific hypothesis that they are important in evaluation of the health, vigor, and quality of other individuals and thereby influence mate choice and competitive interactions. This project integrates mechanistic and functional approaches to olfactory communication. In a more general context, this research demonstrates some of the higher-order mechanisms involved in social perception and characterizes in a unique way the kinds of sophisticated processes animals may use to evaluate one another. Such higher-order knowledge of other individuals are widespread throughout the animal kingdom, which in turn suggests that this kind of evaluation of others has been important in the evolution of complex social behavior necessary for complex social organization. Understanding this kind of higher-order social cognition is necessary if we are to truly understand both the evolution of social communication and the neural mechanisms underlying social recognition, social memory, and social behavior in animals and in humans.

DESCRIPTION (Adapted from applicant's abstract): The goal of this proposal is to understand the neural mechanisms of social recognition and memory. This information will lead to a more thorough understanding of the brain, especially sensory processing by the olfactory and vomeronasal systems, higher-order perceptual and cognitive processes involved in pattern perception, recognition, similarity judgments, and the formation of multi-component representations. In addition, the research will provide a new, unique perspective on the functional neuroanatomy of memory by investigating the role of various brain loci in social memory. Understanding of the brain, and especially of social recognition and memory processes, is relevant to the understanding of many types of human disabilities due to stroke or head injury, and also to understanding the deficits caused by a variety of degenerative diseases, including Alzheimer's disease and Korsakoff's syndrome. The specific aims of the study are to use the extensive knowledge obtained about social communication in hamsters as a model system to investigate the neural mechanisms of recognition of individuals, kin, sex, and reproductive state by odors. There are four specific goals. First, the role of the hippocampal system in discrimination and recognition of individuals will be investigated using lesions and histological methods to determine the brain areas involved and Fos histochemical methods to determine particular groups of cells that are activated during recognition and memory processes. Second, the role of the medial amygdala in sex and reproductive state recognition will be investigated using the same methods. Third, the roles of the hippocampal system (including entorhinal cortex, para-hippocampal area and peri-rhinal cortex) and of the pre-frontal agranular insular cortex in higher-order processes such as multi-component representations of individuals will be examined. Fourth, the functional neuroanatomy of kin recognition will be examined, particularly the similarities and differences between recognition of kin by familiarity and recognition of kin by phenotype matching. These experiments will provide new and unique knowledge about the neural basis of social recognition and social memory that should provide a compelling complement to what is known about other types of learning and memory. They will also provide a basis for finer-grained anatomical and neurophysiological investigations of these processes that are so crucial to the lives of animals and humans.

Olfactory communication by scent marking: from functions to neural mechanisms

Robert E. Johnston

Although much is known about communication by visual and acoustic signals, little is known about communication by odors, yet this form of communication is of primary importance for the social behavior many animal species. The time is ripe for increased investigation of olfactory communication.
Scent marking is one of the primary means by which animals communicate by odors. This research investigates the hypothesis that some forms of scent marking a form of competition through which individuals advertise their relative vigor and genetic quality by scent over-marking. Evidence suggests that other individuals evaluate these over-marks and use this information for mate choice decisions or during aggressive encounters. Studies to test these hypotheses will be carried out in the laboratory and in nature. Other laboratory experiments will be carried out on the perceptual mechanisms involved in interpreting scent marks and in the areas of the brain responsible for marking behavior and for evaluating scent marks.
In summary, a multi-faceted approach will be taken to understand communication by scent marking and odor signals. This work will increase our understanding of the sense of smell, communication by odors, social behavior in animals, and the neural mechanisms underlying social and emotional behavior.

For decades, scientists have been intrigued by how animals recognize the species-specific vocalizations used in social communication. Auditory signals are processed and recognized along the auditory system in the brain. However, vocal recognition must also involve the activation of other brain regions that affect the internal state of the receiver, and subsequently, modulate the behavioral responses to vocal signals. To address this question, the researchers are studying ultrasonic vocalizations (USVs) produced by the golden hamster in a sexual context, and behavioral and neural responses to these vocalizations. Both male and female hamsters exhibit a diverse vocal repertoire during sexual encounters. The hypothesis to be tested in this project is that USVs function in sex recognition, and by activating brain regions involved with reward and motivation, USVs increase sexual arousal and stimulate approach behavior to the sound source. The research tests the hypothesis that behavioral responses are regulated by dopamine, a critical compound in mediating reward. Preliminary data suggest that females vocalize more than males and that female USVs are longer in duration and have broader bandwidth than male USVs. In addition, the vocalizations of both sexes exhibit specific sound features that could indicate levels of sexual arousal and motivation of the caller. This study represents a key innovation in the study of USVs by integrating: 1) acoustic and statistical analyses of USV to demonstrate sex discrimination, 2) playback experiments to validate sex recognition and 3) neural responses to the USVs to reveal the brain regions and mechanisms involved in recognizing the behavioral significance of these USV. Moreover, this study will shed light onto other functions of USVs, which in recent years have become important in understanding social behavior and communication in rodent model species used in biomedical research. The research will also provide research opportunities for STEM undergraduate students.