Do functional neuroimaging studies of SA confirm the Freudian theory of sexual drives? Do they simply reframe it? Or, do they invalidate it and make it obsolete?
As mentioned above, Freud (1915a) acknowledged that theories begin with concepts that are not clearly defined. This is why Freud was so cautious when he introduced the concept of sexual drives. Nobody has ever seen drives under the lens of a microscope; no radiological device has demonstrated their existence as objective entities. When Freud was writing that no science began with clear and sharply defined basic concepts, he was to introduce the concept of sexual drive, which refers to the inferred basis of a subjective experience as contrasted with an observed objective entity.
Although, drives per se are not conscious, the psychoanalytical theory of sexual drives provides a very good account of the conscious phenomenology of sexual desire: indeed, the conscious experience of sexual desire is consistent with the existence of sexual drives that exert pressure for motor expression, tend to reach an aim, make use of an object and likely have an internal bodily source. By contrast, neuroscience per se cannot provide such a phenomenological account: even if neuroscience could provide a complete and objective description of all the responses of the brain regions to VSS, that description would not convey what it is to feel sexual excitement.
We are trying here to determine whether certain features of the subjective experience derived from sexual drives have objective neural correlates. Sexual drives are the basis of conscious experiences, even if they may secondarily become repressed and unconscious. Thus, the neurophenomenological model could account for at least the conscious aspects of sexual desire derived from sexual drives. Hereunder, we examine each of the four components of the neurophenomenological model and try to indicate how it relates to the Freudian conception of sexual drives. We also consider the inhibitory aspects of the model and examine their relations to the Freudian theory regarding the repression and the inhibition of sexual drives.
Here, some terminological clarifications are in order about sexual desire, excitation and libido. By the expression desire, we refer to the felt propensity or urge or impulse to engage in sexual acts. The terms excitement, arousal and excitation encompass more diverse manifestations: they refer to a state where the subject experiences desire and/or bodily changes (genital, respiratory, etc.) and/or cognitive activity (sexual fantasies, plans of seduction, etc.) and/or emotions (joy, apprehension, tension, etc.). Regarding the term libido, “In psycho-analysis […] the term “libido” does not mean psychical energy in general but the motive force of the sexual instincts” (Freud, 1923).
The cognitive component
The experimentally presented visual stimuli are assessed by subjects as to their sexual relevance both qualitatively (“Is this a sexual stimulus?”) and quantitatively (“How sexually arousing is this stimulus?”). Thus, the cognitive component comprises a process of appraisal through which each stimulus is categorized—or not categorized—as a sexual incentive and quantitatively evaluated as such. The target is assessed as corresponding, or not corresponding, to the category of persons to whom the subject is sexually oriented, e.g., adult women in the case of heterosexual males, and, within this preferred category the target is appraised to determine whether or not it presents certain features sexually attractive for the subject (body shape, etc.). In our proposed model, this complex analysis is conceived as performed by various brain regions, including the fusiform gyri and the orbitofrontal cortex. In other words, once the upstream visual areas have analyzed physical characteristics of the objects (gender, body shape, etc.), the assignment of sexual relevance is performed by the inferior temporal and the orbitofrontal cortices, which opens the way to motivational, emotional and bodily responses.
In the proposed model, increased attention devoted to sexually relevant targets is reflected in the activation of regions involved in sustained attention, i.e., the superior and inferior parietal lobules, which are consistently activated in functional neuroimaging studies of visually induced SA (Kühn and Gallinat, 2011; Stoléru et al., 2012; Poeppl et al., 2013; Sescousse et al., 2013).
What is the relationship between the appraisal process of the cognitive component and the object of sexual drives as a psychoanalytic concept, defined as the “thing in regard to which or through which the instinct is able to achieve its aim” (Freud, 1915a)? Such a definition implies that certain categories of “things”—usually other persons endowed with particular characteristics—are experienced by a given subject as stimulating sexual desire. In the proposed model, the inferior temporal and the orbitofrontal cortices are seen as the neural correlates of the operations through which subjects assess stimuli as corresponding, or not corresponding, to the objects of their sexual drives. Clearly, the sexual relevance of visual stimuli is not appraised by individuals as if they were blank screens or tabulae rasae; when they engage in this appraisal process, they have long-standing sexual preferences established during their development. Thus, appraisal is performed in relation to internal references, or memory traces in the language of psychoanalytic theory, which define the characteristics of the objects of sexual drives. The demonstration of hippocampal activation—a key memory area—in a meta-analysis of functional neuroimaging studies of SA is consistent with the view that appraisal is performed in relation to internal references (Poeppl et al., 2013). Thus, in the context of functional neuroimaging studies of SA, the appraisal process can be conceived as the assessment of the match between the external visual stimuli and the internal references. We propose that, while functional neuroimaging studies cannot image the objects of sexual drives, they do image the functional processes through which subjects appraise the match between visual stimuli and the internal references that define the objects of their sexual drives.
The motivational component
Once a visual target is perceived as sexually relevant, a motivational value gets attached to it. This process makes stimuli highly salient, attractive and “wanted” (Robinson and Berridge, 1993). The motivational component is certainly the most crucial aspect of the model. Actually, the term “drive” itself refers to this motor aspect, as a drive is something that tends to make subjects move. Importantly, motivational processes are interfaced with cognitive processes. If a motivational process cannot give way to actual behavior, it will tend to trigger the emergence of representations of the behavior, i.e., motor representations. This happens in particular when actual behavior must be inhibited. Thus, although motivational and cognitive aspects are presented separately for purposes of clarity, they are closely related processes.
As is apparent from the definition above, the motivational component corresponds to two core features of drives: (i) the motor factor, i.e., the feeling of a pressure to act in a sexual manner; and (ii) the intermediate aim of drives (see above), i.e., the pattern of action that the drives strive to execute in order to reach satisfaction. As shown below, VSS induce the activation of several areas belonging to the motor system, which is consistent with the above cited Freudian assertion (“Every instinct is a piece of activity”). We now review the evidence that some activated areas are parts of the motivational component and delineate their relation with features of sexual drives.
According to the neurophenomenological model, once visual stimuli have been appraised as sexually relevant, the processing of these stimuli activates premotor areas, which might lead to overt actions if circumstances made it possible and appropriate. Within the context of a neuroimaging scanner, subjects cannot perform sexual actions so that motor processes are conceived as activating the premotor stage and the representational/cognitive aspects of motivational processes. The activation of the premotor stage could account for the observed widespread activation of the supplementary motor areas, of the ventral premotor areas, and of the region corresponding to the cingulate motor areas (Kühn and Gallinat, 2011; Stoléru et al., 2012). The activation of these premotor areas is linearly correlated with the level of perceived SA (Redouté et al., 2000). In domains other than sexuality, the activation of premotor areas has been related to conscious motor intention (Haggard, 2005).
The ventral premotor area and the supplementary motor area have distinct functions. The lateral premotor cortex—to which the ventral premotor area belongs—uses information from other cortical regions to select movements appropriate to the context of the action (Purves et al., 2001). Its neurons seem to be particularly involved in the selection of movements based on external events. In subjects presented with VSS, activation in the ventral premotor area may reflect externally triggered preparation of movements.
The medial premotor cortex, to which the supplementary motor area belongs, also mediates the selection of movements. However, this region appears to be specialized for initiating movements specified by internal rather than external cues. In contrast to lesions in the lateral premotor area, removal of the medial premotor area reduces the number of self-initiated movements a monkey makes, whereas the ability to execute movements in response to external cues remains largely intact (Shima and Tanji, 1998). Imaging studies suggest that in humans this cortical region functions in much the same way. For example, PET scans have shown that this region is activated when subjects perform motor sequences from memory (i.e., without relying on an external instruction; Grafton et al., 1998).
In keeping with the notion that activation of premotor areas are correlates of the representational/cognitive aspects of motivational processes, their activation has been interpreted as the neural correlate of sexual motor imagery reported by subjects after the presentation of VSS (Mouras et al., 2003; Stoléru et al., 2003; Moulier et al., 2006). VSS do trigger the activation of areas belonging to the neural network mediating motor imagery (inferior parietal lobules, left ventral premotor area, right and left supplementary motor areas, cerebellum). Although “sexual motor imagery” is an expression used in neuroscience, this expression refers actually to experiences that are close to, if not identical with, conscious sexual phantasies, at least to those phantasies where subjects appear as active. While the production of phantasies does not belong to the four core features of sexual drives as described by Freud, he does refer to this production in countless passages of his works (e.g., Freud, 1905, 1920, 1921).
Finally, it has been proposed that the activation of the ventral part of the lateral premotor cortex reflects the increased activity of mirror neurons (Stoléru et al., 1999; Bocher et al., 2001; Ponseti et al., 2006; Mouras et al., 2008). Mirror neurons are a particular class of visuomotor neurons, originally discovered in the monkey premotor cortex, that discharge both when a monkey performs a particular action and when he/she observes the same action performed by another monkey (Rizzolatti and Craighero, 2004). Thus, the activation of these neurons in the observer’s brain mirrors the activation of the corresponding neurons in the observed agent. The theory of the function of the mirror neurons has been expanded to the domain of emotion to account for empathy. Furthermore, we have suggested that a similar mechanism mediated by the mirror-neuron system prompts the observers of VSS to resonate with the motivational state of other individuals appearing in visual depictions of sexual interactions, with observers activating motor representations associated with the observed depictions (Mouras et al., 2008). This interpretation is reinforced by the fact that VSS also induce an activation of the inferior parietal lobule, another region that contains neurons belonging to the mirror-neuron system. These considerations may be important to explain the mechanisms of the widespread attraction to pornographic movies.
Some post-Freudian psychoanalysts, notably the Lacanian school, have elaborated the concept of identification to the desire of the Other: “The object of man’s desire, and we are not the first to say this, is essentially an object desired by someone else” (Lacan, 1953). The potential activation of the mirror-neuron system in response to VSS may thus represent neural correlates of the tendency to emulate the manifestations of sexual desire observed in others, whether directly or through films. This finding suggests the possibility that processes of identification with significant others involve not only identification with their ego or superego functions, but also with aspects of their id. Importantly, this aspect of desire is not well accounted for by the structural model of the psyche (id, ego and super-ego). As the super-ego is commonly conceived as working in contradiction to the id, e.g., maintaining our sense of morality and proscription from taboos, it does not accomodate sexual desire as an identification with aspects of the id of significant others. We propose the concept of super-id as a way to conceive that aspect of desire. This concept, grounded in functional neuroimaging studies of sexual desire, might be a way in which they could help psychoanalysis to further specify certain aspects of the theory of sexual drives.
Another area implicated in conscious motor intention and found activated in functional neuroimaging studies of SA is the posterior parietal cortex. In patients undergoing awake brain surgery, experimental stimulation of the posterior parietal cortex (Brodmann areas 39 and 40) triggered a strong intention and desire to move, e.g., stimulating right parietal regions induced the desire to move the contralateral hand, arm, or foot (Desmurget et al., 2009). Brodmann area 40 was found activated, or positively correlated with penile erection in many neuroimaging studies of SA (Kühn and Gallinat, 2011; Stoléru et al., 2012). This activation could be a correlate of the participants’ expressed desire to perform sexual actions in response to VSS, e.g., the same actions as those depicted in the clips (Redouté et al., 2000).
In the ACC, premotor areas are located in the region identified as the cognitive division (Picard and Strick, 2001). From our perspective, cingulate motor areas are particularly relevant as they may represent an interface between the limbic and the motor systems. The role of the caudal ACC in motor function is known to be similar to the role of premotor and supplementary motor area cortices (Dum, 1993). In the monkey, stimulation of the ACC elicits genital manipulation of a masturbatory character (Robinson and Mishkin, 1968). In human partial seizures with motor sexual manifestations (such as pelvic thrusting), the origin of discharge has been located in the ACC (Landré et al., 1993). The consistently observed response of the caudal ACC to VSS (Stoléru et al., 2012; Poeppl et al., 2013; Sescousse et al., 2013) is thus in keeping with the conclusion that the caudal ACC plays a crucial role in the initiation of goal-directed behaviors (Devinsky et al., 1995), which includes sexual behavior. However, in the neuroimaging paradigms used to study SA, where the urge to act conflicts with the instruction to withhold any overt behavior, there must be control mechanisms at least as powerful as the motivational processes. Activation in the caudal ACC was found in a study of a GO/NO-GO task (Kawashima et al., 1996). More generally, it is activated when there is conflict between possible responses (Carter and van Veen, 2007). According to Picard and Strick (2001), a specific part of the cingulate sulcus [located at y = 24 mm ± 7 mm (mean ± SD, in Talairach coordinates)] appears to be involved in conflict monitoring. Interestingly, several studies on SA have reported activation in this area (Stoléru et al., 1999; Arnow et al., 2002; Karama et al., 2002; Moulier et al., 2006; Safron et al., 2007; Sundaram et al., 2010), which suggests that this activation may correspond to conflict monitoring. Accordingly, we propose that the activation of the caudal ACC in response to VSS results from conflicting inputs to this area: inputs of the GO type, correlated with the perceived urge to enact SA, and inputs of the NO-GO type, correlated with the perceived need to withhold any overt sexual behavior in the current circumstances. Both types of inputs would be associated with activation, because it is the local synaptic activity that is energy consuming.
On the one hand, the neurobiological account of SA proposes a conflict between two kinds of inputs; on the other hand, an essential characteristic of sexual excitement is a “peculiar feeling of tension of an extremely compelling character”(Freud, 1905). The activation of the above described region of the ACC may thus represent a neural correlate of the experience of sexual tension.
While cortical regions are associated with the motivational component, this component also includes subcortical areas. The latter areas are important as they may lead to the causation of sexual desire and to the sources of sexual drives, better than do cortical areas. In animals, the medial preoptic area has repeatedly been implicated in sexual motivation or sexual behavior in males (e.g., Swanson, 2000; Hull and Dominguez, 2006; Balthazart and Ball, 2007) whereas the ventromedial nucleus of the hypothalamus is important for the expression of female sexual behavior, in particular, the lordosis reflex (Pfaff, 1999). In an experiment performed in monkeys (Oomura et al., 1988), the rate of discharge of neurons in the medial preoptic area of an experimental male increased when he viewed a receptive female and performed button presses resulting in bringing the female close to him. In humans also, areas activated in response to VSS include the medial preoptic area (Stoléru et al., 2012; Sescousse et al., 2013).
In response to VSS, the ventral striatum (nucleus accumbens) was found activated in about a quarter of functional neuroimaging studies of SA (27.0%), a rather low percentage given its widely reported involvement in animal studies of sexual motivation and in studies of other motivational processes. Nevertheless, this region was found in a meta-analysis of brain responses to VSS (Sescousse et al., 2013). In functional neuroimaging studies of SA, the level of activation in the ventral striatum was also found correlated with the degree of perceived SA (Redouté et al., 2000; Walter et al., 2008). Two main interpretations of this activation have been proposed. Firstly, it has been conceived as the neural representation of received reward, as VSS are experienced as rewards in themselves (Sabatinelli et al., 2007; Walter et al., 2008; Sescousse et al., 2010). Secondly, this activation has been related to the incentive motivational aspects of VSS and to anticipated reward (Ponseti et al., 2006). But what exactly does “reward anticipation” mean in terms of subjective experience? It may mean the cognitive operation whereby a subject knows that a specific rewarding outcome is going to occur. It may also denote the craving or desire associated with such knowledge.
By contrast, the head of the caudate nucleus (dorsal striatum) has been found activated much more consistently (Stoléru et al., 2012; Poeppl et al., 2013; Sescousse et al., 2013; Figure 3). This region belongs to the nigrostriatal pathway, a dopaminergic (DA) pathway connecting the SN with the striatum (see below). As part of a system called the basal ganglia motor loop, this pathway is involved in the production of motor behavior. We shall also describe in more detail how the head of the caudate could also play a role in inhibiting the expression of overt sexual behavior, once SA has been induced (see section Inhibition of Overt Behavioral Expression). As in the case of the ACC, the same structure could contain both neurons involved in triggering sexual behavior and neurons that tend to inhibit its expression.
What is the relationship between, on the one hand, the motivational component just reviewed and, on the other hand, the pressure factor as a core feature of sexual drives? In domains other than sexuality, the brain areas of the motivational component are known to be correlates of intentional behavior and/or motor imagery. Some of these areas are cortical. At this “higher level” of motivational processes, it is likely that the motor factor (i.e., the urge to move) and the goal of actions (conceived as the conscious imagery of specific patterns of action) are integrated into the desire to perform specific patterns of action. In other words, we propose that the conscious imagery of specific actions and the urge to perform them are correlated with the activation of the cortical regions of the motivational component, with an integration between the urge felt and the representation of the pattern of actions. Thus, what Freud described as two distinct aspects of sexual drives—the motor factor and the intermediate aim of drives—may be integrated into a single entity, namely the pressure to perform specific actions, and correlated with the activation of a single neural network.
It has recently been proposed to distinguish brain regions involved in the representation of pleasure and those involved in the causation of pleasure (Berridge and Kringelbach, 2013). The same distinction between causation and representation could be useful in the case of motivation. Both animal and human studies indicate that the DA neurons located in brainstem nuclei—mainly in the ventral tegmental area (VTA) and the SN—are key elements of motivational processes in general, i.e., not specifically of sexual motivational processes. These general motivational processes rely on DA pathways that appear essential in the causation of sexual motivation. Hereunder, we briefly describe the main DA pathways, and point out their possible involvement in SA and relation with sexual drives as conceived by Freud.
In the nigrostriatal pathway, perikarya arise in the SN and project to the caudate nucleus and the putamen, known collectively as the striatum; nigrostriatal DA neurons are involved in the initiation and execution of copulatory movements (Hull et al., 2004). The bilateral activation of the SN and of the caudate nucleus is a consistent finding across functional neuroimaging studies of SA (Stoléru et al., 2012). The activation of this pathway could be a correlate of the pressure factor of sexual drives, i.e., of the urge to perform motor acts in response to sexually relevant stimuli.
In the mesolimbic pathway, perikarya located in the VTA project diffusely to limbic and cortical structures, including the nucleus accumbens, the amygdala, and the ACC. Various theorists have proposed a motivational interpretation of mesolimbic DA pathway functioning (Alcaro et al., 2007). In the framework of incentive motivation theory (Robinson and Berridge, 1993), “incentive salience” is a psychological process that transforms the perception of stimuli, imbuing them with salience, making them attractive, “wanted”, stimuli. In this theory, the mesolimbic dopamine projections attribute incentive salience to the perception and mental representation of events associated with activation of this pathway. Has the mesolimbic pathway been found activated in neuroimaging studies of SA? The activation of the VTA has been reported in some studies, but not consistently. By contrast, more consistent findings have been obtained regarding the involvement of the VTA in rodents’ sexual behavior (Baskerville and Douglas, 2008). VTA activation has been noted, however, in several studies of romantic love (Cacioppo et al., 2012) and in a study of the neural correlates of orgasm (Holstege et al., 2003). While the origin of the pathway, i.e., the VTA, has relatively rarely been found activated, two of its target areas have been consistently found activated: the ACC and the amygdalas (Figures 2, 3 and 4). However, although amygdalar activation has been related to motivational processes (Hamann et al., 2004), according to current interpretations (Murray, 2007; Walter et al., 2008) the amygdala would process the emotional aspects rather than the motivational relevance of VSS (see below: “The emotional component”).
Like the mesolimbic pathway, the mesocortical pathway originates in the VTA but terminates in the cortex, in particular in the frontal lobe. A recent study supports the view that activation of the VTA and SN regions induced through sexual or romantic imagery could result in widespread cortical activation (Sulzer et al., 2013). Participants were trained to control the level of activation in a region encompassing the SN and the VTA. To achieve this control, real-time fMRI provided subjects with a visual feedback of their SN/VTA activity while they were imagining rewarding scenes—actually sexual or romantic imagery. To examine the effect of neurofeedback, subjects were assigned to either a group receiving feedback directly proportional (veridical feedback) or a group receiving inversely proportional (inverted feedback) to SN/VTA activity. In both groups, sexual or romantic imagery was associated with activation of the SN/VTA region and with activation in frontal, parietal, temporal and occipital cortices. In both groups, analysis showed increased connectivity of the SN/VTA region with the dorsal and ventral striatum; surprisingly, functional connectivity between the SN/VTA region and widespread cortical areas was demonstrated only in the inverted feedback group. If the involvement of the mesocortical pathway in SA is confirmed, it could provide an anatomical basis for the widespread cortical activation associated with SA. This cortical activation could in turn help understand the generation of sexual thoughts and imagery associated with sexual motivation.
Interestingly, a parallel can be drawn between the concept of libido and the idea that sexual thoughts are fueled by mesocortical DA projections. Just as the libido can become attached to different objects (across various persons and during one person’s life history), it is easily conceivable that mesocortical projections establish synapses wih various cortical networks (across individuals or during one individual’s history) giving rise to various object representations associated with sexual desire. Mesocortical projections might then be the support of libidinal cathexis. Similarly, sublimation—directing some proportion of libido on to cultural aims—could be understood as the establishment of new synapses between mesocortical axons and neurons involved in intellectual or artistic cognitive processes. Furthermore, fixations of the libido could be better understood through the concept of long-term potentiation of synapses of mesocortical and mesolimbic neurons. Finally, the idea that libido is a “quantitatively variable force” (Freud, 1905) could be related to the width of arborization and rate of discharge of mesocortical and mesolimbic neurons. Conversely, irrational and primary process thoughts might depend on the impact of DA innervation of cortical networks.
Thus, functional neuroimaging studies of SA suggest that there exists a hierarchy of neural structures and processes whose activation correlate with the experience of the motor factor of drives and the associated motor imagery. The prominent role of the DA pathways in motivation suggests they may be—to use Freud’s terms—an answer biology has returned to the questions psychoanalysis has put to it regarding the source of sexual drives, seen by Freud as “the most obscure part of the psychoanalytic theory of drives” (Freud, 1920). However, the DA pathways subserve not only sexual motivation but also other types of motivation (including eating and drinking). The major difference between the Freudian and the neurophysiological views regarding the source of sexual drives is that psychoanalysis locates these sources in peripheral organs, with sexual excitations arising in certain parts of the body. By contrast, neurophysiology suggests that the source of drives could lie in the brain itself. In the neurophenomenological model, excitations originating in the body do not appear to be necessary for SA to occur, at least in the case of VSS and in adult subjects.
However, the neurophenomenological model may be constrained by its reliance on studies based for their great majority on VSS, which are external stimuli. In addition, regarding the somatic source of sexual drives, it is essential to note that testosterone, secreted by the testicles, has a major impact on sexual motivation. One of the multiple sites of action of testosterone in the brain is the medial preoptic area. In male rats, testosterone increases both basal and female-stimulated dopamine release in the medial preoptic area (Hull and Dominguez, 2006), which possibly enhances sexual motivation. However, Freud’s model of the source of sexual drives as a “process of excitation occurring in an organ” and the hormonally-mediated mechanism just mentioned are different because in the latter mechanism the process of excitation lies in the brain target of testosterone, not in the testicles. Freud himself was aware of emerging knowledge on molecules that would later be called sexual hormones: “It seems probable, then, that special chemical substances are produced in the interstitial portion of the sex-glands; these are then taken up in the blood stream and cause particular parts of the central nervous system to be charged with sexual tension”. He acknowledged the difficulty to integrate his view of erotogenic zones and emerging knowledge on substances produced by gonads: “The question of how sexual excitation arises from the stimulation of erotogenic zones, when the central apparatus has been previously charged” could not be treated, “even hypothetically, in the present state of our knowledge” (Freud, 1905). Moreover, Freud was well aware that in many cases sexual excitement could occur in the absence of sex glands, which showed that testicles cannot be considered as the sole source of sexual drives.
The emotional component
From a phenomenological standpoint, the emotional component includes the specific hedonic quality of SA, i.e., the pleasure associated with rising arousal and with the perception of specific bodily changes, such as penile erection. In our functional neuroimaging studies, the highest ratings for pleasure were associated with the presentation of the most sexually arousing pictures (Moulier et al., 2006; Mouras et al., 2008). Other emotional responses, such as sexual tension or disgust, may occur as part of SA. In the proposed model, the activations of the uppermost part of the primary somatosensory cortex—that receives inputs from the external genitalia—, of the left secondary somatosensory cortex, the amygdalae, and the insulae are conceived as neural correlates of the emotional component (Figure 2)
The prevailing interpretation of the activation of the amygdalae is that they receive multimodal sensory inputs and participate in the evaluation of the emotional content of the complex perceptual information associated with VSS (Ferretti et al., 2005). Then, they relay processed information to the ventral striatum, hypothalamus, autonomic brainstem areas, and the prefrontal cortex.
The level of activation of the insulae was found correlated with the level of markers of SA—penile tumescence or perceived SA (Kühn and Gallinat, 2011; Poeppl et al., 2013). Given the involvement of the insulae in visceral sensory processing (Craig, 2003), the correlation between their level of activation and the penile response may reflect the role of the insulae in the perceptual processing of penile inputs (Moulier et al., 2006) and possibly in the awareness of erection, which would be akin to the insular function of interoceptive awareness (Craig, 2003). This role of the insulae in the sensory processing of penile inputs is consistent with the report that manual stimulation of the penis strongly activates the right posterior insula (Georgiadis and Holstege, 2005).
In the Freudian view of sexual excitement, the emphasis is laid on the concept of sexual tension and on its opposite, sexual satisfaction. The goal of sexual behavior is to reach satisfaction through the elimination of that tension, as satisfaction can only be obtained by removing the state of stimulation at the source of the instinct. Importantly, preliminary sexual activities are themselves accompanied by pleasure and on the other hand they intensify both the excitement and the tension. For instance, “A certain amount of touching is indispensable (at all events among human beings) before the normal sexual aim can be attained. And everyone knows what a source of pleasure on the one hand and what an influx of fresh excitation on the other is afforded by tactile sensations of the skin of the sexual object” (Freud, 1905). In an incremental cycle, such fresh excitation leads subjects to further sexual activities that themselves generate increasing pleasure, tension and excitation. As noted in the first section, Freud recognized this peculiar mixture of tension (unpleasure) and pleasure.
Do neuroscientific findings account for this emotional duality of SA? This duality is reminiscent of research conducted in rodents to disentangle neural circuits involved in pleasure (“liking”) and in motivation (“wanting”). These studies have focused mainly on feeding, but also on sex behavior. They show that mesolimbic dopamine, which was widely considered the brain neurotransmitter candidate for pleasure two decades ago, turns out not to cause pleasure or “liking”. Rather, dopamine mediates more selectively a motivational process of incentive salience, which is a mechanism for “wanting” rewards but not for “liking” them (Berridge and Kringelbach, 2013). By contrast, opioid and endocannabinoid neurotransmitters do more effectively generate intense pleasures—but only within so-called “hedonic hotspots”. For example, stimulation of mu opioid receptors within a hotspot of the nucleus accumbens (a hotspot localized in the rostrodorsal quadrant of the medial shell of the nucleus accumbens), or in another hotspot of the ventral pallidum (in the posterior half of ventral pallidum), more than doubles the intensity of “liking” reactions elicited by sweetness. But the same stimulation of mu opioid receptors elsewhere in the remaining 90% of the nucleus accumbens generates only “wanting” without enhancing “liking”—much like dopamine. Thus, these studies indicate that affects of pleasure and motivational responses are related to specific and distinct subcortical structures. Each hotspot is only a cubic millimeter in rats; then, a human hotspot equivalent should be approximately a cubic centimeter, if scaled to whole-brain size. Importantly, the posterior ventral pallidum was found to be activated in a meta-analysis where no restriction was imposed on the size of clusters of activation concordant across neuroimaging studies (Stoléru et al., 2012; x, y, z: −24, −10, 0, MNI coordinates, unpublished finding). The right nucleus accumbens was also found activated in one of the meta-analyses (Sescousse et al., 2013).
Although orgasm is an essential aspect of the emotional component, we shall not attempt to relate this experience to its potential neural correlates. One reason is that orgasm is not an essential part of Freud’s theory of sexual drives. In addition, functional neuroimaging studies of the neural correlates of orgasm have yet to overcome many difficult methodological problems which have prevented the emergence of consistent results. However, clinical neurology has shown that orgasm can occur in female and male patients as a consequence of lesions in the temporal lobe and/or temporal lobe epilepsy. As an example, a 44-year-old woman experienced for a period of 3 years recurrent episodes in which she would suddenly become aware of a feeling indistinguishable from an orgasm (Reading and Will, 1997). An electroencephalogram showed a right frontotemporal epileptic focus. Radiological examinations revealed a large vascular abnormality in the right temporal lobe. Antiepileptic drug therapy put an end to the occurrence of seizures and to accompanying orgasms. Although rare, such cases have a great theoretical importance because they show that orgasm may occur both in women and men in the absence of any genital stimulation. Thus, a pattern of brain activation, independent of the stimulation of any erotogenic zone, can result in orgasm.
The autonomic and neuroendocrine component
The autonomic and neuroendocrine component consists in the bodily changes that result from sexual stimulation, including genital, respiratory and cardiovascular responses. These changes also include hormonal responses, such as a rise in blood testosterone levels, which has been recorded in men and in all other mammals so far studied, from rats (Bonilla-Jaime et al., 2006) to bulls (Katongole et al., 1971). These autonomic and hormonal changes are understood as preparing the body for copulation. Furthermore, some of these changes, e.g., genital sensations, further contribute to SA, thus generating a positive feedback loop. According to the model, activation in the ACC, anterior insulae, putamens and hypothalamus participates in the mediation of the autonomic and neuroendocrine responses of SA.
This set of bodily changes is distinct from what Freud called the somatic source of sexual drives. They are consequences of the brain processing of sexual stimuli, not the cause of SA. However, in particular in the case of erection, the perception of bodily changes is part of a positive feedback loop where arousal contributes to further arousal. As seen above, midbrain regions (SN, VTA), which provide the origins of DA pathways, could play an essential role in the causation of sexual motivation. In that case, the source would be located in the central nervous system rather than in peripheral organs. Of course, this central mechanism would not eliminate the role of external stimuli and peripheral receptors, but it would mean that these inputs, in and by themselves, are not the source of drives. In a brief passage, Freud acknowledged the existence of a centrally conditioned sensation of sexual stimulation: “The state of being in need of a repetition of the satisfaction reveals itself in two ways: by a peculiar feeling of tension, possessing, rather, the character of unpleasure, and by a sensation of itching or stimulation which is centrally conditioned and projected on to the peripheral erotogenic zone” (Freud, 1905). This passage sounds like a forerunner of the “as if body loop” of the theory of somatic markers (Damasio, 1996) where reasoning and decision-making about a factual situation is influenced by a concomitant “somatosensory image” that defines an emotional response. The somatosensory image is related to a somatosensory activation that can occur in one of two ways: (i) via a “body loop”, in which emotion can be evoked by actual changes in the body that are then projected to the somatosensory cortices or (ii) via an “as if body loop”, in which top-down signaling from regions such as orbitofrontal cortex and amygdala drives activity in somatosensory maps from within the brain, independently of actual body signaling. Similarly, in the domain of sexual desire, actual body loops or “as if body loops” may be activated so that the subjective perception of a given episode of arousal does not remain undifferentiated but is imbued with a specifically sexual character. In that case, the body would not be the source of sexual excitation but would function as a marker of the sexual character of arousal.
If, as posited by Freud, sexual drives are exerting a constant pressure to get expressed behaviorally, and if the SN/VTA is a neural correlate of the source of drives, the SN/VTA should contain neurons which are firing tonically, except after satisfaction has been reached. Indeed, in vivo rodent and monkey VTA and SN DA neurons display basal tonic firing rates of up to 20 Hz (Radulescu, 2010). This view predicts that these neurons should show decreased rates of firing during the sexual refractory period. Unfortunately, the neural correlates of that period are not well known. In the only fMRI study of sexual satiety (Mallick et al., 2007), the amygdalas, temporal lobes and septal area were more active 3 min after ejaculation than after 30 min. As the latter duration was considered as longer than the postejaculatory refractory period, the above-mentioned activations might be neural correlates of the refractory period, leading to hypothesize that these areas might exert inhibition on SN/VTA neurons.
Our review of the last two components of the model leads us to the following questions: Is it tenable that “the sources of sexual drives are somatic processes which occur in an organ or part of the body”—in particular in erotogenic zones (Freud, 1915a)? What is an erotogenic zone in the light of functional neuroimaging studies of SA? Can we maintain that the pleasure derived from the stimulation of an erotogenic zone such as the clitoris or the penis has its source in these organs, or should we rather consider that genital inputs reach brain regions that generate pleasurable sensations? To answer these questions, it is important to consider the brain targets of genital afferents. Using a trans-synaptic viral tracer in order to provide a full map of the functional genitosensory pathway in rats, Normandin and Murphy (2011) have observed viral labeling in the paraventricular nucleus of the hypothalamus in both sexes. Viral labeling was also observed in males, but not in females, in the SN, VTA, thalamus, central amygdala, anterior insular cortex and in the ventro-orbital cortex. All these regions demonstrated in the rat have been found activated in meta-analyses of the neural correlates of human SA in studies predominantly based on visual—not tactile—stimuli (Stoléru et al., 2012). Thus, while tactile genital stimuli converge on areas similar to those that process VSS, genital stimuli may not have a special function as sources of sexual drives. In addition, in humans, as shown by a meta-analysis of functional neuroimaging studies of subjective pleasantness (not limited to sexuality), two of the brain areas found in the rat study, the medial orbitofrontal cortex and the left thalamus, were among the neural correlates of pleasure (Kühn and Gallinat, 2012). Thus, while pleasurable sensations seem to arise in the genital organs, actually the pleasurable character is probably the result of central stimulation triggered by inputs from the genitals.
The above reasoning refers to the hedonic, “liking”, aspects of genital sensations. Should the same reasoning be applied to the motivational, “wanting”, aspect of genital inputs? The answer is likely positive as experiences of centrally mediated genital pleasure are learned and motivate future sexual pleasure seeking. In addition, genital organs may function as somatic markers of sexual motivation, much as other body parts do in the case of emotional responses. Thus, genital sensations may inform subjects on the sexual nature of their motivational state, just as acceleration of heartbeat help them to realize and label their feelings of fear, tension in the jaws their feelings of anger, and stomach sensations their feelings of hunger. However, these body parts are not, in and by themselves, the sources of those emotional or motivational states. In summary, while genital organs with an adequate innervation are important components of sexual pleasure and desire, the final generation of pleasurable sensations and sexual motivation depends on their target brain regions.
The inhibitory components
The proposed model comprises three distinct inhibitory components.
Tonic inhibition from temporal cortical areas
Sigmund Freud was the founder of psychoanalysis, simultaneously a theory of personality, a therapy, and an intellectual movement. He was born into a middle-class Jewish family in Freiburg, Moravia, now part of Czechoslovakia, but then a city in the Austro-Hungarian Empire. At the age of 4, he moved to Vienna, where he spent nearly his entire life. In 1873 he entered the medical school at the University of Vienna and spent the following eight years pursuing a wide range of studies, including philosophy, in addition to the medical curriculum. After graduating, he worked in several clinics and went to Paris to study under Jean-Martin Charcot, a neurologist who used hypnosis to treat the symptoms of hysteria. When Freud returned to Vienna and set up practice as a clinical neurologist, he found orthodox therapies for nervous disorders ineffective for most of his patients, so he began to use a modified version of the hypnosis he had learned under Charcot. Gradually, however, he discovered that it was not necessary to put patients into a deep trance; rather, he would merely encourage them to talk freely, saying whatever came to mind without self-censorship, in order to bring unconscious material to the surface, where it could be analyzed. He found that this method of free association very often evoked memories of traumatic events in childhood, usually having to do with sex. This discovery led him, at first, to assume that most of his patients had actually been seduced as children by adult relatives and that this was the cause of their neuroses; later, however, he changed his mind and concluded that his patients' memories of childhood seduction were fantasies born of their childhood sexual desires for adults. (This reversal is a matter of some controversy today.) Out of this clinical material he constructed a theory of psychosexual development through oral, anal, phallic and genital stages. Freud considered his patients' dreams and his own to be "the royal road to the unconscious." In The Interpretation of Dreams (1900), perhaps his most brilliant book, he theorized that dreams are heavily disguised expressions of deep-seated wishes and fears and can give great insight into personality. These investigations led him to his theory of a three-part structure of personality: the id (unconscious biological drives, especially for sex), the superego (the conscience, guided by moral principles), and the ego (the mediator between the id and superego, guided by reality). Freud's last years were plagued by severe illness and the rise of Nazism, which regarded psychoanalysis as a "Jewish pollution." Through the intervention of the British and U.S. governments, he was allowed to emigrate in 1938 to England, where he died 15 months later, widely honored for his original thinking. His theories have had a profound impact on psychology, anthropology, art, and literature, as well as on the thinking of millions of ordinary people about their own lives. Freud's daughter Anna Freud was the founder of the Hampstead Child Therapy Clinic in London, where her specialty was applying psychoanalysis to children. Her major work was The Ego and the Mechanisms of Defense (1936).