The following page deals with some micropsychological aspects of human sexuality. It is a preprint of a paper published in: Electronic Journal of Human Sexuality, Volume 16, June 9, 2013 www.ejhs.org
THE ROLE OF THE AMYGDALA IN THE DEVELOPMENT OF SEXUAL AROUSAL
Salu, Y. Ph.D
Department of Physics and Astronomy
Supported in part by FacNet, Howard University.
Sexual-arousal is a process that is essential for the survival of the species. The development of its underlying neural networks and their input and output units is genetically controlled, starting in the fetus and maturing at puberty. The mental programs that control the process are learned, and they depend on the person’s experiences and innate make-up. These programs identify arousers based on their gender and on other stimulating qualities that they possess. The programs are recorded in the brain as changes of synaptic weights.
The mental programs are developed unconsciously during childhood, based on non-sexual experiences. At puberty, they are ready to control the activity of the mature sex organs. After puberty, newer programs are learned, based on sexual experiences.
Like in many other behaviors, the unconscious development of these mental programs is based on conditioning. They evolve from root unconditioned stimuli (US) and root unconditioned responses (UR). (A dog can develop elaborate behavior patterns based on the taste of food (the root US) and salivation (the root UR)). A recent model has suggested that the pitch of human voice is the innate root US, based on which a person learns to identify the sex of another person. A combination of the feelings of fear and safety is the innate root US, based on which sexual-arousal emotions evolve. Elaborate sexual-arousal behaviors that vary from person to person emerge from these innate roots, which are common to all humans. The amygdala is involved in sexual-arousal due to the fear and safety emotions, which are parts of this process. This article presents the rationale for the model and for the role of the amygdala, and discusses related experimental findings.
At the end of their childhood, youngsters experience a new sensation - sexual arousal. Some become sexually aroused by men, some by women, and some by both. Different people are aroused by different features of their arousers, but the bodily response and the overall experience of all the aroused are similar. During childhood, as the development of the sex organs is being genetically orchestrated, the mental aspects of sexual-arousal are developing unconsciously based on non-sexual experiences. While explicit and implied instructions by others may have some effects on it, it appears that the broad nature of sexual-arousal depends on the innate make-up of the individual.
A model that describes how the mental component of sexual-arousal evolves during childhood has been proposed recently (Salu, 2011). This model treats the entire process as a learning activity in which a brain program is built by biological mechanisms, based on individual experiences. The brain program has two groups of inputs: features of people based on which their sex can be determined, and features that induce the emotional part of sexual-arousal. The model assumes that there are root cues, common to all people, which the brain is innately hard-wired to detect. Based on the root cues, the individual’s brain learns additional cues that depend on the societal environment in which the individual grows up. The learned cues may vary from one person to another. The root cues have to be robust and universal, to guarantee that everyone could be sexually-aroused at puberty, no matter where and when they happen to live.
The main learning mechanism of the individual cues is conditioning; a group of widespread innate mechanisms that enable animals to adapt to various environments. In conditioning, an animal learns new behaviors based on cues to behaviors that it already possesses.
Classical conditioning is an innate learning mechanism, first described by Pavlov in 1927. Since then, more variants of it were described. It involves, on one hand, a stimulus and its triggered response (the unconditioned stimulus (US, food) and the unconditioned response (UR, salivation)), and, on the other hand, a conditioned stimulus (CS, bell’s ring). When the CS appears in conjunction with the US and its triggered UR, the CS too becomes a trigger of the UR (the bell’s sound triggers salivation). In other conditioning paradigms, activities too can be learned. For example, if an owner whistles as the dog is approaching, and then rewards the dog, the dog will learn to come to the owner’s whistle. In this case, a stimulus-reward pair elicited the linkage of a stimulus and an activity. If a whistle happens to be associated with a flash of light, and the animal is trained to respond to the whistle, it will respond also to the flash of light, with little or no training. The learning pace in conditioning depends on the emotional strength of the learned events. Events with higher emotional strength (positive or negative), are inseminated faster than events with lower emotional strengths. This is, in essence, how innate conditioning mechanisms build individualized complex behavior patterns. Conditioning is crucial for survival, because it enables animals to learn new behaviors that fit the environments in which they happen to be.
The underlying physiology that supports conditioning consists of a root neural network, whose input is the root US and the output is the root UR. Due to the conditioning, synaptic weights are modified between associated stimuli and/ or associated responses and the elements of the root network. As a result, an expanded neural network is created, that supports the original and the learned behaviors. It was demonstrated that humans and other animals can learn new sexual behaviors by conditioning (Klucken et al., 2009).
Innate Brain Wiring and Root Cues
The pitch of human voice
The innate network based on which sexual arousal develops has a root cue for identifying the gender of the arouser and a root cue for generating the emotions of sexual-arousal. According to the model (Salu, 2011) the root cue for identifying the gender of the arouser is the pitch of human voice. The human auditory and vocal systems have some dimorphic properties. The voice of women is different from the voice of men, and men’s brains do some sound processing differently than women’s. There are also some differences that are correlated with sexual orientation (McFadden, 2011). Since the root US’s have to be robust and universal, and since the auditory and vocal systems are designed at the gene level, a model was constructed, suggesting that the pitch of the human voice is the US that the brain uses for learning to distinguish between the sexes (Salu, 2011). According to this model, the sex-activation centers (the UR’s) of most boys are innately tuned to high pitch (women’s) voice (the US’s). The sex-activation centers of most girls (the UR’s) are innately tuned to low pitch (men’s) voice (the US’s). As a result, at puberty, most boys are sexually attracted to women, based on learned cues (CS’s) that have been associated with the women’s high pitch voice. Similarly, most girls at puberty are attracted to men. Homosexual attraction at puberty emerges in boys whose innate sexual UR’s were tuned to men’s voice. It emerges in girls whose innate unconditioned sexual responses were tuned to women’s voice.
Fear and safety in human interactions
The root cue for creating the emotion of sexual-arousal is a combination of the innate emotions of fear and safety (Salu, 2011). This can be discerned by analyzing a variety of sexual activities.
Sex-games are sexual interactions in which the emotions of the participants are in the open. In those games, the players enact non-sexual real life situations, such as a master and a slave, a nurse and a patient, a prisoner and a guard, a rider and a horse, etc. The players become sexually aroused by their mental interaction, even without physically stimulating their sex organs.
The two players in a sex-game may be of the same or of opposite sexes. One of the players (the top) is in control of the other (the bottom). The players please each other, and because of that each feels safe with the other. The bottom is aware of the superiority of the top, and of the top’s ability to harm him/ her. This is a fear-creating situation. So, the emotion of the bottom is a combination of the feelings of safety and fear towards the top. The top, too, feels a combination of safety and fear. The safety is due to his/ her superior position. The fear is more subtle. It may come from his/ her empathy with the feelings of the bottom. It may also come from a deep rooted instinct that any other person has to be approached with apprehension.
These games have a lot in common with pre-puberty evolvement of sexual-arousal, because both relate sexual-arousal with non-sexual events.
Depending on their details, such behaviors may be benign or harmful. According to the DSM IV – TR (APA), such behaviors are considered a mental disorder when: “…The person has acted on these urges with a non-consenting person, or the sexual urges or fantasies cause marked distress or interpersonal difficulty.”
Such combinations of fear and safety feelings towards each other can be found also in other sexual situations. For example, top and bottom body positions, and other expressions of body language during intercourse convey similar messages as those that are conveyed by top and bottom roles in sex-games.
During courtship, the prospect of rejection and the comfort of togetherness have elements of fear and safety emotions.
The wiring of the root neural network
The model (Salu, 2011) assumes that in the innate wiring of the root network, auditory and emotional information are merged and trigger sexual-activation brain centers, such as the hypothalamus. The amygdala is involved in handling the emotional information. After conditioning, the root network is expanded and can process other cues that were associated with the root cues.
The Role of the Amygdala
Comparing the activities of the amygdala in sexual-arousal and in other activities sheds light on its role in sexual-arousal.
The limbic system handles emotional aspects of behavior. The amygdala acts as a hub in the limbic system. It forms connections with an extremely diverse array of structures including cortex, striatum, some thalamic and hypothalamic nuclei, as well as various basal forebrain structures and brainstem nuclei. As a result, the amygdala is in a position to influence a wide variety of processes from autonomic and motor control to memory formation and neuromodulation (Pape & Pare, 2010). In general, the amygdala is involved in the association between a stimulus and its emotional value. This is especially important in decision-making and in triggering autonomic responses to emotional stimuli (Gupta, Koscik, Bechara & Tranel, 2011).
The amygdala has been implicated in processing mental aspects of sexual-arousal in adults. Brain fMRI’s of subjects watching erotic videos were compared with fMRI’s of the same subjects watching non-erotic videos. Due to the complexity of the events, many brain areas were activated by the videos. However, in most studies the activation of the amygdala showed a positive correlation with the erotic stimuli and with the ensuing sexual-arousal (Stoleru et al., 2012; Sundaram et al., 2010; Ferretti et al., 2005; Karama et al., 2002; Hamann, Herman, Nolan & Wallen, 2004; Ball et al., 2009; Bechara, Damaio, Damasio & Lee, 1999). In some studies, such a correlation was not found (Hu et al., 2008).
For decades, the amygdala has been known to be a major player in processing fear information. It is involved in fear-related innate and learned stimulus-response activities, in appetitive processes, and in information storage and retrieval (Gupta, Koscik, Bechara & Tranel, 2011).
Classic studies of animal and human lesion research have identified the amygdala as a critical structure for the expression and perception of innate fear. For example, macaque monkeys have innate fear of snakes. Macaque monkeys that receive amygdala lesions at any stage of their life do not show later-on fear of snakes (Emery et al., 2001; Zola-Morgan et al., 1991; Kluver & Bucy, 1939).
Numerous animal studies have investigated fear acquisition and extinction by conditioning. In a basic paradigm, a noxious stimulus, such as a mild electric shock, is associated with a benign stimulus, such as a flash of light. While intact animals learn the association (or extinguish it as the case may be) and behave accordingly, animals with damaged amygdala fail to learn (or extinguish) the association (Gupta, Koscik, Bechara, & Tranel, 2011).
In certain complex learned behaviors, fear seems to be the underlying innate emotion from which an advanced complex emotion has evolved. For example, people get a bad feeling when they lose money, are betrayed, or when someone they oppose wins the election. These emotions are learned, and they all have a trace of the innate fear. Increased amygdala activation has been found in reaction to losing (and winning) money (Bechara, Damaio, Damasio & Lee, 1999; De Martino, Camerer & Adolphs, 2010; Zalla et al., 2000). Also, research in patients with unilateral amygdala damage reveals that such patients have abnormal responses to defections or betrayals of trust (Koscik & Tranel, 2011). Political candidates elicited in the bilateral amygdala of their supporters stronger responses than in the amygdala of non-supporters. When Japanese and American subjects had to indicate their favorite candidate based on the candidates’ pictures and other pertinent information, the amygdala of both groups showed a stronger response to cultural out-group faces than they did to cultural in-group faces. However, this was unrelated to their voting decisions (Rule et al., 2010).
In MRI studies, greater liberalism was found to be associated with increased gray matter volume in the anterior cingulate cortex, whereas greater conservatism was associated with increased volume of the right amygdala (Kanai, Feiden, Firth & Rees, 2011).
A patient with focal bilateral amygdala damage displayed defective real-world decision-making as seen by inappropriate social behavior (e.g., flirtatiousness with strangers), inability to maintain employment, and inability to maintain stable interpersonal relationships (Adolphs, Tranel, Damasio & Damasio, 1995).
The amygdala was found to be involved also in events where safety is an issue. There are two kinds of feeling safe. One is when an ongoing fear stops. The other is a positive emotion that does not require the pre-existence of fear. In the first kind, firing amygdala cells that respond to fear cues stop firing as the fear stops. As for the second, single cell recordings from basal amygdala cells of freely behaving rats demonstrated that different neurons react to different fear-safety combinations. Some neurons responded selectively to fear cues. Others responded selectively to safety cues. Still others responded selectively to simultaneous fear and safety cues (Sangha, Chadick & Janak, 2013). fMRI studies of social phobics revealed that the amygdala of both social phobics and controls responded to pictures of angry and happy faces by increased activity. However, different brain circuits processed threatening and accepting faces (Starube et al., 2005).
These were just a few of the very large number of studies about the amygdala. In a nut-shell, they demonstrate that the amygdala participates in the development and the execution of a wide array of fear and safety brain programs. These programs handle a spectrum of emotions, starting with robust, innate fear and safety, all the way to complex learned emotions in which fear and safety are only a hint. That may explain the involvement of the amygdala in social behavior. At its core, social behavior is about appraising and responding to situations that involve other people. Each participant wants to feel safe during the interaction, but there is always an inherent risk in it, which depends on the nature of the interaction. In this respects, sexual interactions are a sub-group of social interactions. In some of them, the presence of the fear and safety emotions is obvious; in others, it is indirect.
Sexual-arousal is only the first stage of sexual activity. After it has been triggered, the conditions of the surroundings have to be considered, before the sexual activity can take place. Like in other behaviors, the amygdala has been implicated in interacting with cognitive brain circuits and integrating an internal call-for-action with assessing the involved risks. These assessments may end up quashing the arousal.
Consider a toddler whose sex-activation brain centers are innately tuned to women’s voice. He is now next to his mother as she is talking with another woman. He feels safe next to his mother, but he is somewhat apprehensive of that stranger; to him she looks big and unfamiliar. In general, he is experiencing a combination of safety and fear in the presence of a person who speaks in a high pitch. That triggers the learning of sexual-arousal cues by conditioning. His brain picks up features from the situation, which later in life will serve as sexual-arousal cues. After repeated experiences like this, representations of classes and their cues evolve in his brain. One such class is ‘women’, and its cues include the original high pitch voice and other cues, such as body contours and clothes that are typical to the society where the boy lives. Some of these cues could have been picked up when a woman was not talking, based on their association with other learned cues that identify a woman. Also, non-sexual situations that have undertones of fear-and-safety become cues of sexual arousal when enacted in a sexual context (e.g. a guard and a prisoner in a sex-game). Social skills that the boy develops become new sexual-arousal cues, due to their associations with fear and safety (e.g. controlling or obeying another person), and so on.
At puberty, this child will find himself to be sexually aroused by women. (Similar developments happen in other combinations of boy or girl vs. men or women).
In addition to learning by conditioning, children learn new sexually related information by being told. This information is merged into the information structures that are being built unconsciously by conditioning. After puberty, new sexual-arousal cues are learned from actual sexual activities. These cues do not rely on the feelings of fear and safety.
The mental component of sexual-arousal that emerges at puberty evolves from non-sexual experiences during childhood. It depends on two kinds of learned cues: those that identify the sex of another person, and those that create the emotions that accompany sexual-arousal. The physical component of sexual-arousal is triggered and maintained by the mental component, together with programs that handle information about the surroundings and feedback information from the sex organs.
A theoretical model that describes the pre-pubertal development of the mental component of sexual-arousal has been presented here. The model is consistent with a wide array of experimental observations, typical ones are cited here. According to the model, sexual-arousal evolves unconsciously by conditioning during childhood from non-sexual experiences. The pitch of human voice is the US based on which the cues for identifying the sex of an arouser evolve. A combination of the innate emotions of fear and safety constitute the US, based on which the emotions of sexual-arousal evolve. Information that children are taught by others is merged with this core of pre-pubertal information structure. After puberty, information gained by sexual experiences expands the information structure.
The amygdala is an important brain center that handles various aspects of fear and safety. It is involved in learning new cues, in creating memory records, and in supporting information retrieval in other processes. The model suggests that the amygdala is involved in sexual-arousal through its handling of fear and safety information. Another tenet of the model, which is corroborated by experimental findings, is that the information structures that support sexual arousal are built by conditioning. The model illustrates how conditioning of non-sexual experiences creates the cues for sexual-arousal.
The model suggests a feasible combination of basic biological processes that emulate the observed characteristics of the mental component of sexual-arousal. More studies are needed to ascertain that these are the processes that the brain actually uses. fMRI and electrical measurements may be able to further clarify the connections between auditory pathways that process the pitch of the voice, the amygdala, and sex-activation centers such as the hypothalamus. fMRI methods may be able to discern commonalities and differences between the amygdala’s activation in situations of fear and safety with and without a sexual dimension. Psychological assays may be able to track the roles of fear and safety in social behavior in general and in sexual-arousal in particular.
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