Thesis
Reference
How dirty is the quick and dirty pathway? early spatiotemporal dynamics for the processing of biologically relevant stimuli
LEGRAND, Lore
Abstract
We aimed to unfurl how dirty the quick and dirty pathway is. This subcortical pulvinar-amygdala pathway, bypassing cortical areas, is proposed to be dedicated to fast and crude processing of behaviourally relevant stimuli. We hypothesized that stimuli targeting the innate drive to mate are processed automatically, independently of attention and awareness.
In a first EEG experiment we established that body processing is reflected as a N1 deflection around 150ms post stimulus onset in conscious and unconscious viewing conditions.
Secondly, we recorded intracranial field potentials from the amygdala of a hemianopic patient that differentiate affective from neutral content at latencies faster than 100ms. Last, we functionally imaged that stimulus processing of behaviourally relevant stimuli (bodies and faces) is preserved in a long-term completely cortically blind patient. We conclude that a subcortical pathway operating independently from striate input appraises stimuli alluding to mating opportunities, giving rise to affective blindsight for bodies.
LEGRAND, Lore. How dirty is the quick and dirty pathway? early spatiotemporal dynamics for the processing of biologically relevant stimuli. Thèse de doctorat : Univ.
Genève et Lausanne, 2014, no. Neur. 123
DOI : 10.13097/archive-ouverte/unige:95043 URN : urn:nbn:ch:unige-950431
Available at:
http://archive-ouverte.unige.ch/unige:95043
Disclaimer: layout of this document may differ from the published version.
1 / 1
1 Members of the thesis committee:
Professor Alan John Pegna, PhD, thesis supervisor
Laboratory of Experimental Neuropsychology (LenPsy) Neuropsychology Unit / Neurology Clinic
Geneva University Hospital 1211 Geneva 14 - Switzerland and
Faculty of Psychology and Educational Science University of Geneva
1211 Geneva 4 – Switzerland
Professor Dr. Jean-Marie Annoni
University of Fribourg Neurology
Chemin du Musée 5 CH-1700 Fribourg
Professor Didier Maurice Grandjean, PhD
Neuroscience of Emotion and Affective Dynamics lab (NEAD) Department of Psychology and Educational Sciences
University of Geneva 40 bd Pont d’Arve 1205 Geneva and
Swiss Center for Affective Sciences University of Geneva
Campus Biotech 9, Chemin des Mines CH-1202 Geneva
Dr. Serge Stoléru, PhD
INSERM U 669 Hôpital Paul Brousse 16 Avenue
Paul Vaillant Couturier 94807 Villejuif Cedex France
2 Acknowledgements
I would like to express my gratitude to the Professor Alan John Pegna. As my PhD advisor, Alan has provided me with the most outstanding and rare research opportunities. While providing excellent scientific advice he has always left me the freedom of choosing research interests and carrying out different projects. I was also given the opportunity to profit from him being a brilliant neuropsychologist, sensing the patients’ problems instantly, and leading sophisticated clinical work. Additionally, I will always remain impressed on how he commands an audience. I am grateful for his PhD and laboratory leadership style being supportive, flexible and creating an invariably good atmosphere with his excellent humour.
Alan impresses and reaches everyone’s heart on the spot and I thank him for my exclusively wonderful PhD time.
I would also like to thank the following people;
Professor Jean-Marie Annoni, with whom I was in contact first and thanks to whom I then joined the Laboratory of Experimental Neuropsychology.
Professor Didier Grandjean and Serge Stoléru for being members of my jury.
Maryll Fournet, my PhD long ghostwriter in French; Miralena Tomescu for proof reading my thesis and both for a beautiful friendship.
Liliane Legrand, my impressive and wise mother, for having provided me with the most enriching opportunities and highest life standards.
Nathalie Goetschi and Cristina Bonsignori for invaluable friendship.
3 table of contents
Abstract ... 5
Abstract [en français] ... 6
Introduction [roots & routes] ... 7
aim of the research ... 7
1. the klüver bucy syndrom: roots ... 8
2. the quick and dirty pathway: routes ... 9
3. visual processing theories ... 11
3.1. neuroanatomy of affective vision ... 11
3.1.1. high road: Milner-Goodale. Haxby. Ellis-Lewis. ... 11
3.1.2. low road: LeDoux ... 13
3.2. electrophysiology of affective vision ... 14
3.2.1. high road: Lamme ... 14
3.2.2 low road: mimicking blindsight ... 16
4. neuro-cognitive emotion theories ... 18
5. four component neurophenomenological model of sexual arousal ... 21
6. stimuli ... 25
6.1. fMRI ... 25
6.1.1. supraliminal faces. prosody. food. bodies ... 25
6.1.2. subliminal faces. bodies ... 27
6.2. surface EEG ... 27
6.2.1. supraliminal faces. bodies ... 27
6.3. intracranial EEG ... 30
6.3.1. supraliminal faces. bodies ... 30
6.4. surface EEG ... 30
6.4.1. subliminal faces. bodies ... 30
7. blindsight ... 31
7.1. dorsal route blindsight ... 31
7.2. ventral route blindsight ... 33
8. hypothesis ... 36
Methods ... 38
9.1. “Basic instinct undressed: early spatiotemporal processing for primary sexual characteristics.” (Legrand, et al., 2013) ... 38
9.2. “quick AND dirty: intracranial recording of affective blindsight for bodies” (Legrand, et al., in prep.) ... 38
9.3. “Neural correlates of body and face perception following bilateral destruction of the bilateral visual cortices” (van den Stock, et al., 2014) ... 38
Discussion ... 39
10. hypotheses verification ... 39
11. theoretical implications and future directions ... 40
11.1. four component neurophenomenological model of sexual arousal ... 41
11.1.1. future directions ... 43
11.2. the quick and dirty pathway ... 44
11.2.1. future directions ... 47
11.3. amygdala processing ... 49
11.3.1. future directions ... 50
11.4. blindsight and consciousness ... 51
11.4.1. future directions ... 53
12. upshot of this thesis ... 53
4
5
Abstract
We aimed to unfurl how dirty the quick and dirty pathway is. This subcortical pulvinar- amygdala pathway, bypassing cortical areas, is proposed to be dedicated to fast and crude processing of behaviourally relevant stimuli. As such, we hypothesized that stimuli targeting the innate drive to mate would profit from this automatic processing. Automatic processing is accepted as an effect that occurs independently of attention and independently of awareness in this work, assuming this encompasses that it happens unintentionally and uncontrollably (Schneider & Shiffrin, 1977) . To this end we designed four experiments to elucidate the temporal and spatial dynamics of the processing of biologically relevant human bodies. In a first EEG experiment we established that body processing is reflected as an N1 deflection around 150ms post stimulus onset. This early component in the stream of visual processing is modulated by affective processing, as induced by nude depictions of the preferred sex of the observer. Importantly, this effect arises in conscious as well as unconscious viewing conditions. In a second step we recorded intracranial field potentials from the amygdala gaining maximal temporal and spatial resolution. The patient (LA) whose electrophysiological response pattern was recorded suffers from unilateral cortical blindness.
Hence, the recorded amygdala response occurred independently from striate visual processing. Nonetheless intracranial field potentials in the amygdala proved to differentiate affective from neutral content at latencies faster than 100ms. In other words, we recorded affective blindsight intracranially. An fMRI experiment carried out with the same patient (LA) evidenced sustained amygdala activation in affective blindsight for bodies. Last, we functionally imaged that stimulus processing of behaviourally relevant stimuli (human bodies and faces) compared to behaviourally irrelevant stimuli (car and butterflies) is preserved in another patient with complete cortical blindness (TN) despite long-standing V1 absence.
From this series of investigations we conclude that a subcortical pathway operating independently from striate input appraises stimuli alluding to mating opportunities, giving rise to the phenomenon of affective blindsight for bodies. In summary; the quick and dirty pathway is sensibly dirty.
6
Abstract [en français]
Nous avons investigué la façon dont la voie directe du traitement des informations (« quick and dirty pathway »), est impliquée dans le traitement des contenus affectifs liés à la reproduction. Il a été établi que cette voie sous-corticale pulvino-amygdalienne, contournant les aires corticales, est vouée au traitement rapide et grossier des stimuli comportementalement pertinents. Ainsi, nous avons formulé l’hypothèse que les stimuli ayant trait à la motivation innée de reproduction bénéficieraient de ce traitement automatique. Afin de tester cette hypothèse, nous avons réalisé quatre expériences pour élucider les dynamiques temporelles et spatiales du traitement de stimuli comportementalement pertinents : des corps humains. Dans une première expérience en EEG, nous avons établi que le traitement des corps apparait sous forme d’une déflexion N1 autour de 150 ms après l’apparition du stimulus. Cette composante précoce dans le déroulement du traitement visuel est modulée par le traitement affectif, que nous avons induit par le visionnage de représentations de corps nus du genre préféré de l’observateur. En outre, cet effet se produit dans les conditions de présentation consciente aussi bien qu’inconsciente. Dans un second temps, nous avons enregistré les potentiels électriques intracrâniens via une électrode située au niveau de l’amygdale, obtenant ainsi une résolution temporelle et spatiale maximale, ceci chez un patient (LA) souffrant de cécité corticale unilatérale. Ainsi, la réponse amygdalienne enregistrée s’est produite de façon indépendante du traitement visuel du cortex strié.
Néanmoins, les potentiels électriques intracrâniens au niveau de l’amygdale ont différencié les contenus affectifs des neutres à des latences inférieures à 100 ms. En d’autres termes, nous avons enregistré au niveau intracrânien un « blindsight affectif » unilatéral. Une expérience en IRMf réalisée avec le même patient (LA) a mis en évidence une activation amygdalienne soutenue lors de la présentation de corps dans ce cas de cécité corticale unilatérale affective.
Finalement, nous avons montré par imagerie fonctionnelle que le traitement de stimuli comportementalement pertinents (corps et visages humains) comparativement à des stimuli comportementalement non pertinents (voitures et papillons), est préservé chez un autre patient souffrant de cécité corticale (TN), ceci malgré l’absence de long terme de V1. De cette série d’investigations, nous concluons qu’une voie sous-corticale opérant indépendamment des entrées du cortex strié, évalue les stimuli relatifs aux potentialités de reproduction, ceci expliquant le phénomène de « blindsight affectif » pour des corps. En résumé, la voie directe du traitement des informations se charge également des informations affectives reliées à la reproduction.
7
Introduction [roots & routes]
aim of the research
The research plan was designed to investigate the spatiotemporal dynamics of the processing of stimuli targeting innate and automatic processes related to reproduction. In fact, the drive to mate is on par with the need for nutritional supply and the detection of threat (J. LeDoux, 2012). The latter has received a wealth of researchers attention whereas the homeostatic and reproduction axis of survival related mechanisms was rather neglected. Genetically determined, hard wired neuronal processing mechanisms were hypothesized to be devoted to the assessment of stimuli of particular importance to one’s well being. Maybe not by coincidence, one of these processing pathways is subcortically embedded and is thought to operate automatically, independent of attention and in the absence of awareness (J. LeDoux, 1996). Because of this (c)rude processing manner, not adhering to cortical information processing standards, it was dubbed “the quick and dirty pathway” (J. LeDoux, 1996).
However, the primacy of affect that is allegedly mediated by this pathway and the evolutionary importance is extrapolated from research on emotional facial expressions.
Additionally, the six basic emotions conveyed by facial expressions turned out to be less homogenous in their effects than expected (Ekman, et al., 1987). In a parsimoniously reductionist approach this research aimed at investigating the earliest stage of the drive to mate by means of presenting naked and dressed bodies corresponding, or not, to the sexual preference of the viewer. We were interested in whether these stimuli are also processed automatically, and therefore fast, and independent of awareness. A first experiment was planned to assess whether or not the drive to mate is indeed processed by automatic mechanisms that are robust against consciousness alterations. To this end, healthy subjects were exposed to naked and dressed bodies in conscious (supraliminal) as well as unconscious (subliminal) viewing conditions while simultaneously recording EEG. After asserting the validity of this approach, we investigated the processing of these stimuli by the amygdala, the most prominent candidate to account for these effects. The temporally high resolution but spatially confined dynamics of unconscious processing were evaluated from intracranial depth recordings, and the spatial dynamics in fMRI.
8 1. the klüver bucy syndrom: roots
Tame, hyperphagic, visually agnosic and sexually unappeasable monkeys after bilateral temporal lobes removal in 1939 (Kluver & Bucy, 1997) are at the origin of our understanding of the neural correlates of affective processing. These symptoms form the Klüver Bucy syndrom, named after the surgeons of this intervention. Subsequently, selective inferior temporal lobectomy as compared to amygdalectomy allowed to doubly dissociate the Klüver Bucy syndrom. Inferior temporal lobe removal induced visual agnosia in the absence of the other symptoms whereas fear reduction, hypermetamorphosis and hypersexualty was a consequence of bilateral amygdalectomy (Weiskrantz, 1956). Amygdala ablated monkeys suffered of what Weiskrantz called the “ the amygdaloid hangover”, subsuming the monkeys reduced fear of people and previously aversive stimuli such as sticks and gloves, and their sexual orientation indifferent behaviour. Fear reduction was quantified by the extinction rate of fear responses to a pre-operatively aversively conditioned stimulus. The dark compartment of the monkey’s cage, that they naturally prefer, was conditioned to be avoided through electroshocks (unconditioned aversive stimulus). After surgery, inferior temporal resected and sham operated monkeys still avoided the conditioned dark part. On the contrary, amygdalectomized monkeys did not avoid the conditioned dark department of the cage which proved rapid post-surgical fear extinction. Weiskrantz concluded that his monkeys were indifferent to reinforcing stimuli (psychic blindness) because of a failure to evaluate the stimuli according to their threatening or rewarding properties (Weiskrantz, 1956).
The human homologue of the Klüver Bucy syndrome was soon reported in bilaterally temporal lobectomized epileptic patients (Terzian & Ore, 1955) and amygdala damaged patients due to herpes encephalitis, head trauma and dementia (Hayman, Rexer, Pavol, Strite,
& Meyers, 1998; Marlowe, Mancall, & Thomas, 1975) (B & Sang Yoon). The diagnosis of the Klüver Bucy syndrom requires three of the following symptoms; visual agnosia, hyperorality, hypersexuality (including changing sexual preference), memory deficits or distractibility (Hayman, et al., 1998). These symptoms were almost exclusively observed in bilateral temporal lobe/amygdala patients (Adolphs, Tranel, Damasio, & Damasio, 1995) and were described in adults as well as children (Ozawa, et al., 1997). Conversely, patient SH suffering from the very rare Urbach Wiethe syndrom, a condition with selective bilateral amygdalae destruction (nearly complete in her case), failed to show the Kluver Bucy symptoms. Nonetheless, she was observed to be affectively rigid, always being in a good mood. Following up on Weiskrantzs’ assumption of impaired affective stimulus appraisal after amygdala removal this patients discrimination abilities of emotional facial expressions were investigated (Adolphs, Tranel, Damasio, & Damasio, 1994; Adolphs, et al., 1995).
9 Indeed, the patient was incapable of discriminating fear from other emotional categories and couldn’t rate the intensity conveyed by the emotional expression. Pairing two stimuli belonging to the same emotional category was possible whereas judging which categories are more similar to one another was erroneous (e.g. surprise and anger compared to surprise and happiness). Face identity recognition and learning remained flawless. This suggested that stimulus appraisal involves independently operating processing pathways since patient SH was unimpaired in facial identity recognition, could pair up faces according to emotional category but was affectively incapable of discriminating between different emotional categories.
Thus, these lesion studies neuroanatomically pinpoint the amygdala as being crucially involved in affective appraisal of threat, food and sexual behaviour related inputs. As a matter of fact, even nowadays, neither animals nor humans suffering from a Klüver Bucy syndrom, approaching predators, eating everything at hand and sexually harassing others are likely to survive for long alone. It therefore appears sensible that brains are equipped with more than one pathway to ensure survival (J. LeDoux, 2012). Independently wired routes conveying information to the amygdala were reported to proceed via cortical as well as subcortical structures (J. LeDoux, 1996).
2. the quick and dirty pathway: routes
The reasoning underlying the dual route hypothesis, arguing for a distinction between emotion and cognition is that the processing of a snake as being an edible animal with a skin to make a bag out of is different from the assessment that it is a potentially lethal danger. The evolutionarily based appraisal theory of LeDoux advocates a low subcortical road next to the traditional high cortical road in charge of detailed processing. The low road bypasses cortical areas to operate in a “quick and dirty” manner, making the difference between “the quick and the dead” in case of emergency (J. LeDoux, 1996). Evidence for the latter, detail unburdened, basic stimulus processing stemmed from priming experiments. It had already been shown that subjects can be primed with 1ms presentations of random polygons that they subsequently don’t recognize when presented among new distracter polygons but nevertheless rate to prefer in a “like-dislike” forced choice task (Kunst-Wilson & Zajonc, 1980). No detailed processing of the stimulus occurred since the recognition performance of the subjects was at chance level whereas the favouring of previously presented stimuli argues for crude but very rapid processing of the stimuli leading to subsequent affective discrimination (Kunst-Wilson &
Zajonc, 1980). The crude low route processing is set out to trigger fight or flight responses at useful speed through direct colliculus - thalamus- amygdala projections which in turn outputs
10 its evaluation to behavioural, endocrine (hormone release) and autonomic (blood pressure regulation) structures if necessary (J. LeDoux, 1996). LeDoux experimentally mapped out the processing pathways by lesioning the high road primary auditory cortex (-thalamus- amygdala) as well as the low road colliculus - thalamus- amygdala relay stations (see Fig.1).
Lesion induced alterations were measured by modifications of the rats classical fear conditioned responses. Pavlovian fear conditioning is automatic and reproducible (across species) but extincts in amygdala ablated monkeys (Weiskrantz, 1956) and therefore represents a reliable indication whether information was processed by the amygdala or not.
---
“The neural pathways involved in fear conditioning are well characterized. When the CS is an acoustic stimulus, the pathways involve transmission to the lateral nucleus of the later amygdala (LA=
from auditory processing areas in the thalamus [medial division of the medial geniculate body (MGm/PIN)]
and cortex [auditory association cortex (TE3)]. LA, in turn, projects to the central amygdala (CE), which controls the expression of fear responses by way of projections to the brainstem areas. ANS, Autonomic nervous system; CS, conditioned stimulus; HPA, hypothalamic-pituitary axis;
MGv, ventral division of the medial geniculate body; PRh, perirhinal cortex; TE1, primary auditory cortex”.
---
Fig.1: Auditory high and low road (J. E. LeDoux, 2000)
As hypothesized, primary auditory cortex ablated rats subjected to aversive conditioning by pairing a tone (conditioned stimulus) with a foot shock (unconditioned stimulus) normally expressed their conditioned fear response of freezing, heart rate decrease or drinking suppression (J. E. LeDoux, 2000). Consequently, the conditioned tone must have reached the amygdala through an alternative pathway bypassing the primary auditory cortex.
Subcortically lesioning the auditory thalamus (medial geniculate nucleus), inferior colliculus and basolateral nucleus of the amygdala on the other hand made the rats unresponsive to fear conditioning (J. E. LeDoux, 2000). Neuroanatomical thalamo-cortical-amygdala (high road) and thalamo- amygdala- hypothalamus as well as putamen connections were evidenced by dissecting the horseradish peroxidase stained brains (J. E. LeDoux, 2000). On a temporal scale, single cell recordings in the lateral amygdala showed fear conditioned increased
11 responses prior to cortical auditory responses, lending support to a rapid subcortical processing pathway (Quirk, Armony, & LeDoux, 1997).
On a theoretical level these findings were advanced as evidence that affective processing is neither post-cognitive nor necessarily post-cortical (Kunst-Wilson & Zajonc, 1980).
Visual affective neuroscience embraced this dual route appraisal model and extensive research on whether the mere appraisal of visual affective stimuli in humans is processed via parallel routes was launched. A parallel visual information processing pathway bypassing the primary sensory region seemingly anarchically challenged hierarchical visual stimulus processing models (Andino, Menendez, Khateb, Landis, & Pegna, 2009).
3. visual processing theories
3.1. neuroanatomy of affective vision
3.1.1. high road: Milner-Goodale. Haxby. Ellis-Lewis.
Separate “vision for perception” and “vision for action” pathways is the concept of two routes hierarchically processing visual input along two separate streams proposed by Milner and Goodale (Goodale & Milner, 1992; Milner & Goodale, 2008). V1, the primary visual (striate) receives retinal information from the optic nerve via the lateral geniculate nucleus of the thalamus. From V1, the striate cortex information processing is bifurcated into a ventral route, the “what pathway”, projecting into the inferior temporal lobe and a dorsal route, the “where pathway”, projecting to the parietal lobe. The ventral “what pathway” processes form (V3) and colour features (V4) for object recognition and the parietal “where pathway” responds to movement (V5/MT) to locate objects in space. Hence, both pathways process visual information, ones output being a perceptual representation of an object and the other one coordinating visual guidance for action (Milner & Goodale, 2008). For this reason, patients could suffer from optic ataxia, a deficit characterized by a grasping deficit with intact gnosia, or visual form agnosia albeit intact reaching skills (Milner & Goodale, 2008).
The generic ventral visual processing pathway for object recognition was adapted to account for category specific face processing (Haxby, Hoffman, & Gobbini, 2000). According to this categorical model, face stimuli are decoded by three intra- as well as interhemispherically connected core categorical (faces) hubs in the lateral fusiform gyrus and the superior temporal sulcus (STS). In the hierarchy of visual processing, face parts are processed early on in the occipital face area (OFA) (inferior occipital gyrus). Later in the stream of visual processing, the fusiform face area (FFA) is thought to holistically integrate the parts to a face. Changeable
12 aspects of the face such as the mouth would be processed in the STS. Occipital (OFA) and temporal (FFA) face areas are supposed to be connected along the inferior longitudinal fasciculus (Gschwind, Pourtois, Schwartz, Van De Ville, & Vuilleumier, 2012). The STS was reported to additionally be connected to the anterior temporal pole by the arcuate fasciculus (Gschwind, et al., 2012), thus connecting the core to the extended face processing system (Haxby, et al., 2000). However, selective categorical processing areas have been put into question by showing rather patchy distributions of face selective areas along the inferior temporal lobe as well as a great deal of overlap between stimuli of different categories (eg.
Faces, body parts, natural or artificial objects) (Liu, et al., 2013). By now, it also seems as though this face specific processing model has to be extended to include body stimuli since adjacent as well as partially overlapping with the FFA and OFA, the fusiform body area (FBA) and occipital body area (OBA) was delineated in localizer experiments (Downing, Chan, Peelen, Dodds, & Kanwisher, 2006; Downing, Jiang, Shuman, & Kanwisher, 2001;
Peelen & Downing, 2005a, 2005b, 2007; Schwarzlose, Baker, & Kanwisher, 2005).
The extended system in the model of Haxby provides category unspecific inputs such as face identity and other semantic information by the anterior temporal pole, the intraparietal sulcus for spatially directed attention and the amygdala for emotional processing. In this model the amygdala only connects to the “dorsal route” STS core face region, possibly because evidence was derived from gaze experiments (Davies-Thompson & Andrews; Haxby, et al., 2000; Kanwisher, McDermott, & Chun, 1997). The amygdala was found to be connected to the ventral pathway as well as possibly with direct V1-amygdala long range fiber tracts (Gschwind, et al., 2012). The ventral route-amygdala connection entered the affective face processing model of Ellis and Lewis based on the dissociations between prosopagnosic and Capgras patients. Prosopagnosic patients cannot recognize faces but have affective skin conductance responses (SCR) for pictures of friends and relatives (Ellis & Lewis, 2001) whereas patients suffering from the Capras delusion have no impairment in face recognition but lack the affective component leading to the feeling of familiarity. Patients suffering from the Capgras delusion therefore conclude that their relatives were exchanged, even though they physically look the same (Ellis & Lewis, 2001; Lang, et al., 1998).
Stimuli with an additional affective component were shown to activate the amygdala but also categorical core processing areas such as the FFA for faces (Vuilleumier, Armony, Driver, &
Dolan, 2001). In logical consequence, patients with amygdala sclerosis would lack this effect.
Indeed, it has been shown that epileptic patients with amygdala lesions showed attenuated affective processing induced V1 activations compared to epileptic patients with hippocampal sclerosis (Vuilleumier, Richardson, Armony, Driver, & Dolan, 2004). The notion of the anarchical nature of affective processing amygdala cells in the otherwise hierarchical visual system is supported by these findings. Optionally, cooperating feedback loops between the
13 amygdala and cortical structures have been proposed to heighten the activation to salient stimuli (Gschwind, et al., 2012; Lang, et al., 1998; Vuilleumier, et al., 2004). Neuronal feedforward and feedback processing is introduced in more detail in paragraph 3.2..
3.1.2. low road: LeDoux
LeDoux, introduced here above, is the reference for the concept of a subcortical processing pathway (low road), bypassing primary sensory cortical areas. In human affective vision the automatic and crude assessment of stimuli through the low road would rely on deviating optic fibers that project to the superior colliculus (SC) and pulvinar directly (Grieve, Acuna, &
Cudeiro, 2000). From the SC the information would be conveyed to the pulvinar and directly to the amygdala (Liddell, et al., 2005; Morris, Friston, & Dolan, 1997). Fibers connecting the SC, pulvinar and amygdala have been evidenced by diffusion tensor imaging (DTI) (see Fig.2). It has even been suggested that these fibers possibly run uninterruptedly from the SC- inferior pulvinar to the amygdala (Tamietto, Pullens, de Gelder, Weiskrantz, & Goebel, 2011).
---
---
Fig.2: Reconstructed fiber tracts connecting the superior colliculus - pulvinar and the amygdala (Tamietto, et al., 2011)
14 3.2. electrophysiology of affective vision
3.2.1. high road: Lamme
Visual perception and decision making on a percept have an upper maximal processing time of 150ms. In a go- no go task depending on whether the scene featured an animal or not, a difference between go and no go trials arose over frontal electrodes, a component generated by the no-go decision, the inhibition of a behavioural response (Thorpe, Fize, & Marlot, 1996).
Hence, electrophysiological investigation with a high temporal precision is optimally suited to disentangle visual processing. A temporal pattern based model of visual processing suggests that the incoming stimuli are rapidly processed along the visual hierarchy in a fast
“feedforward sweep” and updated in a second run through “feedback loops” (Lamme, Super,
& Spekreijse, 1998). The notion of an initial feedforward sweep of visual information processing that occurs without stimulus feature integration in V1 is based on the temporal pattern recorded in the different cortical areas. In the macaque brain, V1 activations were recorded as fast as 35ms post stimulus onset, reaching the anterior inferior temporal cortex by 100ms (Lamme, et al., 1998). Between hierarchical levels, such as V1 to V2, latencies of 10ms were recorded. 10ms is also the minimal inter-spike interval of cortical neurons. Hence, it was assumed that a cortical neuron can maximally fire once before the next hierarchical hub (for example between V1 to V2) is reached. This excludes any kind of integration across neurons within one processing hub. In other words, the initial stimulus is gone by the time neurons within V1 can start “talking”. However, basic visual tasks like textural figure-ground segregation, requires multiple orientation selective neurons to integrate their information. It was thus assumed that this integration would be done by a second processing step. This second step would thus depend on recurrent activation and inter-neuron communication. The assumption of recurrent neuronal processing to finish off the stimulus feature integration challenges the notion of a purely hierarchical visual system. Furthermore, it has been assumed that different visual feedforward processing mechanisms, working in parallel could exist (Lamme & Roelfsema, 2000). Cells in V1 and cells in distant cortical areas (frontal eye field, MT) were recorded to fire at the same time after stimulus onset which can only be explained by parallel processing routes.
In humans, reports of temporal patterns of visual processing vary greatly. One of the reasons that could explain the disparity is related to the analysis technique. Because ERPs are not sensitive to high frequency bands, differences in higher frequency bands can be computed by time frequency analysis in the absence of any difference in ERPs (Edwards, et al., 2009).
15 Cortically, electrocorticography (ECoG) recordings were summarized to temporo-spatially follow a P1-N2-P3-N7 deflection pattern for face processing (Allison, Puce, Spencer, &
McCarthy, 1999; Halgren, et al., 1994). This refers to a first positive deflection (P1) that is not specific to faces. Conversely, the N2/P3 components were enhanced the most when faces compared to pictures of other categories such as cars or letter strings were presented. The late N7 component again, is not solely enhanced to pictures of faces. Following the hierarchical pattern, the P1 peaks around 75-100ms over occipital areas (lingual gyrus). The face sensitive N2 peaks around 144-200ms in the ventral occipito-temporal cortex as well as the lateral surface of the temporal lobe. The ventral occipito-temporal cortex, anterior fusiform gyrus and superior temporal sulcus generate a face sensitive later deflection around 350 ms (P3) and at last a negative component starting from 600-700ms on (N7). The early components (P1/N2) are seen as “structural encoding” or “template formation” and later the components as more elaborate processing. A superimposed affective component in the stimulus is discriminated starting from 300ms on, lasting up until 1000ms (Krolak-Salmon, Henaff, Vighetto, Bertrand, & Mauguiere, 2004; Pourtois, Spinelli, Seeck, & Vuilleumier, 2010a). In this broad time range, enhanced cortical implication to affective faces was reported in cortical visual, face and reward processing areas such as the striate cortex (lingual gyrus), face processing specific STS (Allison, et al., 1999), anterior temporal cortex and orbitofrontal cortex (Krolak-Salmon, et al., 2004). Differential ERP enhancements to unpleasant stimuli were additionally recorded in the ACC, hippocampus, inferior parietal lobe, precuneus and the insula (Brazdil, et al., 2009; Puce, Allison, & McCarthy, 1999).
Time frequency analysis of local field potentials in a face sensitive areas in the inferior temporal cortex showed differences in gamma power (68-100Hz) only at 326ms after stimulus onset (Matsuo, et al., 2013). On the other hand, motion stimuli that morph from neutral to affective (fearful/happy) differentiated among emotions as early as 120ms in the fusiform gyrus, as computed by high gamma band power differences (70-150 Hz) (Kawasaki, et al., 2012).
Most interestingly, depth electrodes in the amygdala recorded increased gamma band power as early as 50 to 150 ms after stimulus onset when presented aversive compared to neutral pictures (Oya, Kawasaki, Howard, & Adolphs, 2002; Sato, et al., 2011). Another study reported low gamma band differentiating between emotions starting from 50ms to 250ms and subsequent high gamma increases between 150-250ms and 350-450ms. Because the majority of their recording sites were located in the medial nucleus of the amygdala (compared to lateral, inferior and anterior) they reasoned that these differences do not only reflect visual processing but also reflect visual binding of features with emotional meaning by the medial nucleus of the amygdala (Oya, et al., 2002).
16 Despite all its invaluable advantages, intracranial EEG is inherently incomplete due to punctual tissue coverage and since it is only performed in patients undergoing epileptic or tumor surgery biased by eventual complementary lesions or plasticity that influence the recorded signal. Therefore the unique history of every patient, the various recording techniques (ECoG, depth electrodes, single cell recordings) as well as the different analysis methods might explain the temporal and structural variance across reports. Spatially less precise but more generalizable EEG findings in healthy are discussed in paragraph 5.2..
3.2.2 low road: mimicking blindsight
Blindsight is a condition in which subcortically driven neuronal processing can reliably be investigated. Blindsight arises after V1 lesions that cortically blind the patients and describes
“ a condition in which the sufferer responds to visual stimuli without consciously perceiving them” (Weiskrantz, Warrington, Sanders, & Marshall, 1974). Due to the lesion in the primary sensory cortex, and therefore the visual input and distribution node, the patients are blind and hence not conscious about visual input. This condition separates unconscious from conscious processing. As in blindsight V1 is knocked out, the high road is defeated and visual processing is possibly deviated on alternative routes, such as eventually the low road (Tamietto, et al., 2011). In healthy control subjects, preventing conscious processing of the presented stimuli through masking techniques simulates the blindsight condition of not being aware of a presented visual stimulus. The effect of masking can arise from early disruption within V1 through lateral inhibition by the processing of the mask (Macknik & Livingstone, 1998) or through impaired recurrent access to the striate cortex at a later stage (Fahrenfort, Scholte, & Lamme, 2007). This difference is crucial to the assumption on whether backward masking allows for the investigation of purely low road processing or suffers high road processing contamination. The argument of a disruption of visual processing at the level of V1 was built upon the observation that single cell recordings in the monkeys striate cortex responded to the onset of an unmasked target stimulus but were inhibited when a mask was prepended, referred to as forward masking (Macknik & Livingstone, 1998). Backward masking of a stimulus (the converse stimulus-mask presentation order) suppressed the otherwise occurring target induced after discharges (Macknik & Livingstone, 1998). This data suggests that masking interferes with stimulus processing very early on at the level of V1 and impairs further processing. Doubts about the exclusiveness of mechanisms at play were cast upon it on two grounds. The efficiency of masking depends on the stimulus onset asynchrony (SOA) as well as the duration of the mask. If only V1 cells inhibition accounts for masking it should happen no matter what SOA or duration the mask is. Secondly, responses to masked
17 complex shape targets were recorded in the inferior temporal cortex, implying the stimulus was processed by high level cortical vision (Kovacs, Vogels, & Orban, 1995). Fahrenfort et al. (2007) used less contrasted stimuli for pattern masking than Macknik and Livingstone (1998) and reported suppressed ERP differences in masked compared to unmasked trials after 110ms over occipito-temporal electrodes (Fahrenfort, et al., 2007). Thus, re-activation of occipito-temporal areas was present in the unmasked condition and absent in masked trials.
Ventral visual pathway feed forward processing starts around 40ms in V1 cells. At a later stage these cells were found to be reactivated, showing recurrent processing. The authors conclude that during masking the initial feed forward sweep of neuronal transmission spreads normally and unaltered by the mask. The missing re-entrant feedback however, would truncate conscious visual processing at a later stage (around 100ms) (Lamme & Roelfsema, 2000). Because in the masked condition subjects are not conscious of the presented stimulus, the authors claim that recurrent processing is inalienable for conscious stimulus processing.
Further evidence for this claim was derived from studies applying transmagnetic stimulation (TMS) over the occipital pole. TMS pulses were applied at 100ms after stimulus onset, in the crucial timeframe of re-entrant feedback reaching V1. Although subjects had impaired conscious processing of the stimulus, they nevertheless guessed stimulus properties above chance, as blindsight patients do (Lamme, 2006). The subjects reported not seeing the stimulus but when prompted to guess the orientation or the colour of the “subliminally”
presented patch, their guessing was above chance (Boyer, Harrison, & Ro, 2005).
Supposedly, this could be explained by the fact that at 100ms the stimulus is “gone” with the feedforward sweep but recurrent processing is prevented by the pulse applied at 100ms (Lamme, 2006). Therefore, initial feed forward processing would suffice to guide behaviour and to judge stimulus properties above chance. The disruption of the process at the stage of recurrent processing on the other hand would impair conscious access. However, this plan left the subcortical pathway out of the map. Indeed, the authors tested the hypothesis that feed forward processing and therefore behavioural performances could be disrupted by applying TMS over occipital areas when applied earlier than at 100ms post stimulus onset. The result was that subjects guessed stimulus properties above chance despite TMS applied earlier than 100ms the (Jolij & Lamme, 2005). This outcome strongly argues for an intact and behaviourally important quick and dirty pathway. Notwithstanding, it seems as though affective blindsight could be induced by TMS. In the latter experiment, participants guessed the emotion expressed by the emoticon above chance without being consciously aware of it.
In summary, visual processing is mediated through a ventral and dorsal route structurally encoding and integrating the information to a percept and guiding action in space (Goodale &
Milner, 1992). Human faces and bodies seem to be processed in rather confined cortical areas
18 along the two visual streams, such as the occipital and fusiform face/body area and in the superior temporal sulcus (Peelen & Downing, 2007). These cortical areas appear to be functionally and structurally connected with the amygdala (Gschwind, et al., 2012; Tamietto, et al., 2011). Cortical visual stimulus processing starts around 100ms in occipito-temporal areas (Allison, et al., 1999). Intracranial amygdala recordings show differential processing of affective compared to neutral visual content between 50-150ms (Oya, et al., 2002; Sato, et al., 2011). These early co-occurring processing patterns in cortical areas and the amygdala evidence processing mechanisms that operate in parallel(J. E. LeDoux, 2000). In a second processing stage, cortical and subcortical processing seems to interact as the amygdala was shown to influence occipital processing (Rotshtein, et al., 2010; Vuilleumier, et al., 2004).
Hence, the spatio-temporal aspect of affective processing, initially surmised in early reports of the Klüver Bucy syndrom and descriptions of experiments investigating the dual route hypothesis have now further been elucidated, the cognitive neuropsychological pattern of this temporo-spatial processing and which stimuli are of interest to the quick and dirty processing pathway still stands to reason. Weiskrantzs’ inference that this amygdala centred processing mediates the appraisal of a stimulus according to its rewarding features is supported by a wealth of research reports and summarized in theoretical models as outlined in the next paragraph.
4. neuro-cognitive emotion theories
Emotion theories vary in complexity and categorization approaches of emotional content but they converge on the idea that emotion processing is genetically determined and occurs via parallel processes. “Discrete” emotion theories assume a genetically determined processing of at least four basic emotions across species and humans, as famously stated by Darwin (Dalgleish, 2004). This line of thought was followed up by Paul Ekman. He carried out what Darwin had sought and proved cross-cultural recognition of six basic emotions; fear, anger, happiness, disgust, surprise and sadness (Ekman, et al., 1987). He adheres to discrete emotion theorists believing that basic emotions are processed by separate neuronal systems (Ekman, et al., 1987; Sprengelmeyer, Rausch, Eysel, & Przuntek, 1998). According to this theory, disgust is neuronally separable from happiness processing for example (Davidson, Ekman, Saron, Senulis, & Friesen, 1990). Dimensional theorists on the other hand care little about emotion categories but classify emotions on dimensional scales such as intensity of arousal and valence (pleasant/unpleasant) (Lang, 1995).
Despite not being classified as an emotional theory, it has to be introduced that Freud influentially analysed the psychic apparatus. Divided into the id, ego and super ego, the
19
“psychic apparatus” is partially conscious but majorly operates at the unconscious level (Freud, 1989). According to Freud the psychic apparatus is driven by the unconscious that stores innate drives. The psychic apparatus constantly scans the external environment to update the internal state with external sensory information, recruiting attention resources if needed. This and other psychodynamic assumptions are implemented and updated in various theories, the latter for example also in the component process model appraisal theory.
Emotion theories differ in their perspectives to study affective processing. This can either be a rather neuroanatomically based approach with limited conceptual a priori of underlying cognitive mechanisms and the subjects’ qualia; or a majorly psychologically centred theory with few assumption on neuronal processing. On the other hand, the component process model (CPM) is more exhaustive by accounting and testing the merits of the different approaches. The CPM is evolutionarily outlined according the need of a rapid cognitive- behavioural association to detect and adapt to opportunities and dangers, needs, and goals of the organism (Dalgleish, 2004; Darwin, 1872). This requires interacting but parallel processing pathways that operate consciously and conscientiously as well as unconsciously crude but fast (Freud, 1989; Lamme, et al., 1998; J. LeDoux, 2012). There are different levels of arousal and processing which by their sum ultimately lead to conscious experiences of emotion (dimensional emotion theories (Lang, 1995)). Emotion processing is centred but not restricted to the amygdala (Ekman, et al., 1987; Kluver & Bucy, 1997; J. LeDoux, 2012).
The conclusion of integrating, ordering, developing and testing these approaches clusters emotion processing into 5 components (Sander, Grandjean, & Scherer, 2005) (see Fig.3). A
“cognitive component” evaluates objects and events, a “motivational component” prepares action, and an actual “motor expression” communicates intentions. The “subjective feeling”
component monitors internal states and external interactions and a “peripheral efference component” updates and regulates the system.
---
---
Fig.3: 5 components of the CPM (Sander, et al., 2005)
20 The appraisal process starts with stimulus evaluation checks (SEC) initiated by relevance or salience detection (Sander, Grafman, & Zalla, 2003). The brain is thought to constantly scan the external and internal environment
“[…] for the occurrence of events (or the lack of expected ones) requiring deployment of attention, further information processing, and possibly adaptive reactions” (Sander et al. 2005, p.319).
The initial assessment through SEC was partitioned into a a) novelty check (initiated by sudden onset of a stimulus or familiarity with the stimlulus), b) intrinsic pleasantness check depending on genetically fixed schemata and overlearned associations resulting in pleasure or pain, independent of momentary preferences or goals, as well as c) a goal and relevance check, aligning motivational priorities. In this model, the “urgency check” triggering fight or flight appraisal based responses results from the second step, the implication assessment. The subcomponents of this second stage of appraisal are self-explanatory and consist of a a) causal attribution check, b) outcome probability check, c) discrepancy from expectation check, d) goal/need conduciveness check.
Stimulus evaluation checks (SEC) volley through three levels of processing (see Fig.4). These are scaled from an initial crude assessment (quick and dirty) to a conscious appraisal of goal conduciveness or obstructiveness with cortical implication (detailed high road processing).
The first level of processing is activated by novel intense stimulation by stimuli targeting innate preferences (sensory motor level). These are subsequently matched to schemata such as learnt preferences and acquired needs (schematic level) and at the highest level of processing evaluated in terms of conscious goals.
---
---
Fig.4: Levels of processing for SEC (Sander, et al., 2005)
This initial assessment could be carried out automatically and in the absence of awareness up until the schematic processing level, meaning that it covers innate as well as learnt preferences and aversions. The conceptual level, involving cultural meaning systems on the other hand would be mediated by cortical association areas.
21 This model assumes sequential processing whereby the different processes are sequentially initiated but not necessarily terminated for the next step to be launched. Thus, the CPM is a sequential processing model with a high degree of parallel subprocessing. In sum, the CPM and the dual route theory are both appraisal theories and converge on the aspects that affective content is processed in parallel and subserved by a fast and crude as well as a cognitively effortful detailed assessment. The mechanisms responsible to ensure emotional precedency are innate and can thus be observed not only in adults but also in newborns and primates. Last but not least, it is agreed that the level of processing determines the stimulus’
degree of consciousness.
The mechanisms are neuroanatomically centred around the amygdala mediating relevance detection (Sander, et al., 2003) but make up the subjects “qualia” (feeling of emotion) through
“fuzzy activation propagation” (Sander, et al., 2005).
The appraisal of primary reinforcers, such as sexual stimuli, and neuroanatomical fuzzy activation propagation giving rise to the qualia of sexual arousal was conceptualized in the four-component neurophenomenological model of sexual arousal by Stoléru et al. (Stoleru, et al., 1999). The appraisal of a stimulus with sexually incentive value induces the expectation of reward and eventually states of craving (Stoleru, Fonteille, Cornelis, Joyal, & Moulier, 2012). Sexual arousal, entailed by this initial appraisal, is a complex psychological and physiological state with a wide range of neuroanatomical processing mechanisms (Stoleru, et al., 2012). This phenomenological and neuroanatomical model of sexual arousal is of particular interest because it was mainly developed on research conducted on visually induced sexual arousal. Because of the particular focus of this thesis on very early affective visual processes, the model is reported in greater detail for the cognitive and emotional component whereas the motivational as well as neuroendocrine and autonomic component are only briefly sketched. On the other hand, because the involvement of the amygdala in visual affective processing is detailed more comprehensively in the next chapter, it is not discussed within the four-component model.
5. four component neurophenomenological model of sexual arousal
The appraisal of a stimulus as being a sexual stimulus is part of the cognitive component of the four component neurophenomenological model of sexual arousal of Stoléru et al. (Stoleru, et al., 1999). Sexual arousal was defined as the physical and psychological readiness to perform sexual behaviour (Stoleru, et al., 2012). Sexual arousal could be triggered by external
22 stimuli or without any external apparent cause and can be of psychological and/or physical nature (Stoleru, et al., 2012).
The cognitive component (1) acts in concert with the emotional (2), motivational (3) and neuroendocrine and autonomic component (4). The cognitive aspect of appraisal and categorization of a stimulus as being a sexual stimulus might be the bottleneck component upon which the other three components depend. The cognitive appraisal was reviewed to direct attention towards the desirable stimulus and induce motor imagery. Successful identification of a desirable stimulus would entail the other components that are activated in parallel rather than sequentially. The emotional component is thought to evoke the hedonic
“qualia” of sexual arousal, that is, the pleasure associated with rising arousal and the perception of bodily changes such as penile tumescence. The motivational component directs behaviour to a sexual goal and is perceived as the urge to express overt sexual behaviour. The neuroendocrine and autonomic component would physiologically prepare the organism for sexual behaviour, inducing cardiovascular, respiratory and genital changes. These components are interrelated and can all be modified by an inhibitory component as schematically outlined in figure 5.
---
Abbreviations: ACC (anterior cingulate cortex); Ant (anterior); Comp (component); Cx (cortex); Inf (inferior);
IPL/SPL (inferior/superior parietal lobule); OFC (orbitofrontal cortex); PMv (ventral premotor area); post (posterior); SI/SII (primary/secondary somatosensory cortex); SMA (supplementary motor area); SN (substantia nigra)
---
Fig.5: Four-component neurophenomenological model of sexual arousal, reproduced from (Stoleru, et al., 2012)
The neural correlates of the appraisal of stimuli, the central attribute of the cognitive component, encompass the right lateral OFC and the inferior temporal cortex. The neuronal
23 substrate of the appraisal of sexual stimuli was disentangled from other processes by means of correlation analyses between perceived sexual arousal judgements of the subjects and cerebral blood flow (rCBF) measures. Additionally, rCBF while watching moderately sexually arousing pictures was contrasted to conditions of viewing pictures of no sexual and highly sexual content (Redoute, et al., 2000). In healthy heterosexual men, right lateral orbitofrontal rCBF increases corresponded to moderately sexually arousing depictions of women.
Furthermore, the right orbitofrontal cortex activation didn’t differ among the non-sexual and highly sexual content presentations. Nonetheless, a correlation between penile tumescence and the right orbitofrontal cortex activation was already reported for this initial stimulus processing. Furthermore, the inferior temporal cortex was reported to be enhanced to visual sexual stimuli corresponding to the sexual orientation preference (Paul, et al., 2008).
Videoclips of heterosexual couples engaged in sexual activity yielded increased activations in inferotemporal areas in heterosexual men but not in homosexual men and vice versa for video clips of homosexual couples videos (Paul, et al., 2008). Also this area linearly correlated with penile tumescence measures (Redoute, et al., 2000). The other cognitive task is to orient attention towards the sexually salient stimulus. As for other stimuli prompting attention attraction, the medial intraparietal sulcus was activated in response to visual sexual stimuli (Mouras, et al., 2008). The neuronal cluster mediating motor imagery, the third function attributed to the cognitive component, was reviewed to comprise the inferior parietal lobe, left ventral premotor area, bilateral supplementary motor areas and the cerebellum. In the parietal lobe, somatosensory areas corresponding to the mouth and hands preceded penile tumescence measures by 20s (Mouras, et al., 2008). Inferior parietal but also premotor areas (ventral premotor as well as SMA) were interpreted to be activated during sexual motor imagery mediated by the mirror neurons contained in these areas (Mouras, et al., 2008). Last, in the meta-analysis the cerebellum was observed by several studies presenting visual sexual stimuli (Stoleru, et al., 2012). This finding is on one hand discussed in relation with homeostatic regulations such as the sensation of thirst and hunger. On the other hand the cerebellum is reviewed in the context of a neural network mediating motor imagery.
Then, the emotional component groups various neuronanatomical areas that are implicated in the pleasure associated with rising arousal and the perception of bodily changes. The structures at play are the primary somatosensory cortex for the perception of genital changes, the secondary somatosensory cortex, the right posterior insula and the amygdala. As introduced, amygdala activations to visual sexual stimuli are discussed in the next chapter.
Insula activations correlated with ratings of perceived sexual arousal as well as penile tumescence (Moulier, et al., 2006; Mouras, et al., 2008). Manual penile stimulation induced strong insula activation (Georgiadis & Holstege, 2005). In line with this, epileptic seizure onset in the insula was reported to induce genital sensations (Stoffels, Munari, Bonis,
24 Bancaud, & Talairach, 1980) in (Stoleru, et al., 2012). However, because penile tumescence changes preceded posterior insula activations (Moulier, et al., 2006) it was suggested that this part of the insula would mediate interoceptive awareness, in this case of penile bodily sensations (Stoleru, et al., 2012). The anterior part of the insula was ascribed to the neuroendocrine and autonomic component (preparing the body for sexual action) mainly because the BOLD response to visual sexual stimuli in this case preceded penile responses (Moulier, et al., 2006; Mouras, et al., 2003). Additionally, anterior insula activations were reported to depend on plasma testosterone levels (Redoute, et al., 2005). This latter finding was relied to a report that testosterone secretion would be mediated by the anterior insula in rats (Banczerowski, Csaba, Csernus, & Gerendai, 2001) in (Stoleru, et al., 2012). Otherwise, the correlation between the magnitude of penile tumescence and neuronal activation was most striking in the rostral portion of the anterior cingulate gyrus and the hypothalamus, which were correspondingly judged to belong to the neuroendocrine and autonomic component of sexual arousal (Redoute, et al., 2000).
The motivational component represents the verbally reported urge to act out the sexual desire.
For the neuroanatomical underpinnings, rCBF underlying the viewing of highly sexually arousing stimuli was analyzed. This revealed important activations in the caudal part of the anterior cingulate gyrus, which is reasoned to eventually have been induced by the inhibition of the urge to act out the sexual desire in an experimental context (Redoute, et al., 2000). It is also reviewed that the motivational processing of sexual stimuli could be quite specific to the claustrum and putamen. Furthermore, it is mentioned that the motivational component could partially be mediated by unconscious processes.
As frequently iterated by now, systems for relevance detection would be set to appraise stimuli related to threat, food supply and the drive to mate. Interestingly, the response to food and sexual stimuli follows the same pleasure cycle (Georgiadis & Kringelbach, 2012). It can be summarized in three stages, motivation, consummation and satiety. Anticipating and identifying food as well as sex recruits overlapping neuroanatomical structures such as the phylogentically older lateral posterior OFC, the amygdala, insula, the ventral striatum and the anterior cingulate cortex (ACC). Consummation was reviewed to imply a repeated motor pattern for chewing food as well as during copulation. Tasting flavours as well as orgasm sustains OFC and insular activations. After this process, satiety arises in both cases (Georgiadis & Kringelbach, 2012; Georgiadis, Kringelbach, & Pfaus, 2012).
Furthermore, the restriction on food consumption by anorexics entrains decreased sexual libido, whereas bulimics have increased libido (Reich, 2001). On a neuroanatomical basis, anorexics suffer of amygdala atrophy, which would explain reduced appraisal of desirable stimuli (Friederich, et al., 2012).
25 Amygdala activation related stimuli such as emotional faces, food and sexual stimuli are summarized next.
6. stimuli
6.1. fMRI
6.1.1. supraliminal faces. prosody. food. bodies
Emotional faces prominently trigger enhanced amygdala activation compared to neutral faces, for a meta-analysis of 105 studies on emotional facial expressions see (Fusar-Poli, et al., 2009). Fearful (Ohman & Mineka, 2001), angry (Mattavelli, et al., 2012, 2013;
Sprengelmeyer, et al., 1998) happy, sad and disgusted compared to neutral faces enhance amygdala activations, especially when gaze is directed towards the viewer compared to when it is averted (George, Driver, & Dolan, 2001). Imaging faces expressing fear shows the strongest test-retest reliability compared to other emotions (Sauder, Hajcak, Angstadt, &
Phan). The amygdala is more startled by novel compared to familiar faces (Blackford, Avery, Cowan, Shelton, & Zald, 2011; Gobbini & Haxby, 2006). Introverted subjects have a diminished novel-to-familiar processing ratio due to sustained amygdala activation to familiar faces (Blackford, et al., 2011). Amygdala activation dwindles as a function of decreased trustworthiness (Engell, Haxby, & Todorov, 2007). Along this pattern, autistic as well as Asperger syndrom patients do not show amygdala activation to cut out eyes of different emotions from the mind in the eye test (used to depict patients from autism spectrum disorder) but sustain the activation in fronto-temporal regions (Baron-Cohen, et al., 1999).
The amygdala was thus ascribed a pivotal role in theory of mind processing. In the auditory domain, angry prosody in meaningless speech increases amygdala activation compared to meaningless speech spoken in a neutral voice (Fruhholz, Ceravolo, & Grandjean, 2011;
Fruhholz & Grandjean, 2013). Furthermore, stimuli showing food activate the amygdala, especially when the subjects are in a hungry state (LaBar, et al., 2001). Additionally, amygdala activation is recorded when presented with biological movement compared to random movement (Bonda, Petrides, Ostry, & Evans, 1996).
Importantly, amygdala engagement does not seem to be an all or none phenomenon, being turned on by certain stimulus categories but not by others. It rather appears to work in an adaptive fashion since it habituates over trials (Fruhholz & Grandjean, 2013), underlies test- rest fluctuation (Mattavelli, et al., 2012) and is state dependant given that it gets more activated by pictures of food when subjects are in a starving compared to satiated state (LaBar, et al., 2001). Furthermore, amygdala activation seems to correlate with personality traits. Whereas extroverted subjects seem to activate the amygdala for the appraisal of novel
26 faces, introverted subjects sustain its activity even when faces are repeatedly seen (Blackford, et al., 2011). Nonetheless, a study combining emotion with novelty showed that novel stimuli increase amygdala activation whether of emotional or neutral nature but exclusively for stimuli of human bodies, not scenes (pictures of the IAPS set) (Balderston, Schultz, &
Helmstetter, 2011).
As mentioned above, comparatively little research was carried out investigating the innate axis of the reproductive system and the drive to mate. The conscious appraisal of a stimulus as being a sexual stimulus initiating the first stage of the sexual response cycle (Masters &
Johnson, 1966), the stage of excitement, seems to involve the amygdala, ventral striatum/nucleus accumbens (Georgiadis, et al., 2012), whereas it was found to be deactivated during subsequent genital arousal (plateau) and orgasm (Holstege, et al., 2003). Accordingly, amygdala activation was not correlated with penile tumescene measures (Mouras, et al., 2008). It appears to be re-activated only in the last, the post-ejaculation refraction phase (Mallick, Tandon, Jagannathan, Gulia, & Kumar, 2007). As discussed in Stoléru et al. (2012), this pattern of amygdala activation during the appraisal of a desirable stimulus but deactivation during sexual intercourse corresponds to the pattern observed in the Klüver Bucy sydrom after amygdala lesions. Animals as well as humans have intact sexual behaviour but an indiscriminate appraisal of the possible sexual partners. Further evidence that the amygdala is involved in the appraisal of a stimulus as being desirable can be also be inferred from the study of (Redoute, et al., 2005) who reported that hypogonadal patients who present a decreased sexual drive (libido), showed increased regional cerebral blood flow (rCBF) in the right amygdala, insula and left inferior frontal lobe while viewing pictures of sexual intercourse after pharmacological treatment of their endocrine deficiency. The increased insula, amygdala and inferior frontal gyrus rCBF measures were correlated with higher subjective ratings of sexual arousal for these stimuli after treatment. However, the positive correlation of increased amygdala activation leading to higher attractiveness ratings of the stimuli seems to be reversed in healthy control subjects. Even though women judge couples during intercourse as well as nude depictions of their preferred sex more arousing than men do, men show more bilateral amygdala and hypothalamus activation to visual sexual stimuli than women (Hamann, Herman, Nolan, & Wallen, 2004). From a structural perspective, size seems to matter concerning the amygdala. Unilaterally amygdalectomized epileptic patients who reported postsurgical stable or decreased sexual drive were delineated to have a smaller spared amygdala compared to patients reporting increased sexual drive (Baird, Wilson, Bladin, Saling, & Reutens, 2004).
