Oscillatory Brain Activity in Human Affective Stimulus Processing

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Oscillatory Brain Activity in Human

Affective Stimulus Processing

Dissertation zur Erlangung des Doktorgrades

Eingereicht an der Sozialwissenschaftlichen Fakultät der Universität Konstanz durch

Andreas Keil

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Dank

Der englischsprachige Leser wird mir verzeihen, daß dieser Teil der vorliegenden Arbeit in deutscher Sprache abgefaßt ist. Es scheint auch in der eigenen Muttersprache schon schwer genug, allen Personen gerecht zu werden, die auf ihre Weise zum Gelingen der hier vorgestellten Experimente beigetragen haben. Ich möchte es dennoch versuchen.

Ohne das Engagement und die Hilfe meiner Betreuer, Matthias M. Müller und Thomas Elbert, wäre es nie auch nur zu einem Beginn dieser Arbeit gekommen – vielen Dank! Eine ganze Menge Kollegen haben seit meinen Anfängen in Konstanz im Juni 1997 bis heute versucht, mir etwas beizubringen. Davon habe ich im Rahmen meiner Möglichkeiten profitiert und schulde daher folgenden Menschen grossen Dank: Carsten Eulitz für den ersten richtig guten Tipp und viele weitere Hinweise; Markus Junghöfer und Ursula Lommen für die geduldige Einführung in die Elektrophysiologie; Kelly Snyder für Hilfe beim vorliegenden Mansukript; Olaf Hauk für das bereitwillige Beantworten von Fragen zum ‘Quellenraum’;

Peter J. Lang für geduldiges Diskutieren; Friedemann Pulvermüller ebenso; William J. Ray für kontinuierlichen Unterricht im wissenschaftlichen Schreiben; Edward Taub ebenso; Victor Candia für hilfreiche ad-hoc Kommentare zu Manuskripten und Abbildungen; Luigi für geduldige Hilfe bei Rechnerproblemen; Matthias M. Müller für kontinuierlichen Unterricht in allem und jedem – viel Glück in Liverpool und tausend Dank! Dieser Abschnitt kann nicht beendet werden, ohne meinem Kollegen Thomas Gruber zu danken für seine Geduld und Hilfsbereitschaft. Einen besseren Kollegen kann ich mir auch bei einiger Anstrengung nicht vorstellen. Ebenfalls viel Glück auf den Weg – Du wirst mir fehlen.

Die an der Datenerhebung und -Auswertung beteiligten Hilfskräfte und Diplomanden haben mehr als nur ‘geholfen’. Vielmehr sind zahlreiche Ideen dieser Arbeit aus gemeinsamem Arbeiten und Diskutieren entstanden. Vielen Dank dafür an Klaus Lang, Christine Knöpfler, Angelika Mikuteit, Heidi Messmer, Eva Bonna und Margarita Stolarova.

Ebenso möchte ich den über 80 Studierenden danken, die 2 oder 3 Stunden Zeit ihrer Zeit opferten und engagiert und motiviert an unseren Experimenten teilnahmen.

Die Tatsache, daß dies der letzte Absatz ist, den ich dieser Arbeit hinzufüge, wird meine Familie, meine Eltern und Freunde vielleicht mehr erfreuen als ausladende

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Dankesworte. Dennoch: Allen vielen Dank für die grosse Unterstützung, besonders während der letzten Monate. Außerdem entschuldige ich mich für physische und - schlimmer noch - mentale Absenz. Felix - im neuen Jahr bauen wir wirklich und ganz bestimmt ein Vogelbeobachtungshaus

Konstanz, Januar 2000 AK

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I. Introduction

The present thesis investigates human affective¹ stimulus processing. This element of behavior in humans has been considered an important part of contemporary theories of emotion. Since the focus of this thesis is on physiological mechanisms, namely oscillatory brain activity, biological approaches will be emphasized, with a strong bias towards EEG and behavioral data collected in experiments challenging human emotions in a laboratory environment. However, since the field of emotion research is expanding into a multidisciplinary enterprise, taking into account data from a variety of research areas, I will also discuss both empirical and theoretical aspects of the current thesis in a broader context.

Five experiments are presented covering a wide range of affective stimuli and procedures.

Experiment A employs ambiguous figures allowing for perceptual switches between affectively different percepts; in experiments B, C and D, standardized colored picture stimuli from the International Affective Pictures System (IAPS; Lang et al., 1997) are used, and in experiment E, participants are presented with visual feedback reflecting their performance in an instrumental conditioning paradigm. The dependent variables include the event-related potential (ERP), the Steady-state visual evoked potential (SSVEP), and the visual induced gamma-band activity (GBA). It will be shown that the latter measures may be suitable for examining affective processes and provide convergent as well as complementary information, compared to traditional measures used in experimental psychology or psychophysiology.

Emotion: A brief account on definitions and theories

The concept of emotion is unique in psychological research, in that it has a variety of daily language implications and, due to its relevance in many aspects of human behavior, is also a concept which is frequently used in multiple semantic contexts. Systematic empirical and theoretical evaluation of emotional phenomena requires a definition of ‘emotion’ that allows for at least partial agreement regarding the main characteristics of the problem under consideration. In the following chapter, some of the major theories of human emotional behavior will be reviewed. I will focus on those contemporary approaches that have relevance

1 In this thesis, the terms ‘affect’ and ‘emotion’ as well as ‘affective’ and ‘emotional’ will be used in an interchangeable manner.

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for the question examined here, namely, the psychophysiological aspects of human affective stimulus processing. Three major theoretical contributions that make predictions for emotional modulations of visual perception will be discussed in detail. In addition, the implications of each theory for a definition of ‘emotion’ will be emphasized.

1. Integrative theories on human emotion

The scope of biological approaches to the understanding of emotion has broadened from considering mainly peripheral processes as is the case with James-Lange theory (James, 1890), or alternatively an ‘emotional center’ in the brain as proposed by Cannon-Bard approach (Cannon, 1929). As early as the late 1930’s, proposals such as the Papez loop model or the limbic system theory (MacLean, 1955) have made a strong case for the absence of one emotional center in the brain, focusing rather on interactions between distributed structures (Papez, 1938). It is now commonly accepted that emotions involve the integrated activity of various parts of the central and peripheral nervous system. Furthermore, it appears to be clear that different aspects or forms of emotional phenomena are based on the activity of different biological systems. It remains debatable however, whether these aspects should be theoretically organized into a number of orthogonal basic emotions (Panksepp, 1992) or are better viewed as variations in an emotion space, spanned by a limited number of affect dimensions (e.g. Lang, 1994).

Apart from these considerations, the biological substrate of different emotions has been accessed using a wide range of methods. One theoretical focus has been the description of a physiological affect system and its parts (see Cacioppo and Gardner, 1999, for review).

For example, the relation between neurotransmitter systems and anxiety has been addressed using a pharmacological and animal learning data base (Gray, 1983). Jeffrey A. Gray postulates the existence of three fundamental systems for the regulation of emotion on a behavioral, cognitive/computational and neural level: A behavioral approach system (BAS), a behavioral inhibition system (BIS) and a fight and flight system (FFS). The neural basis of the BIS, in Gray’s view, consists of a widespread network that includes the septo-hippocampal system, the Papez circuit (which includes sensory thalamus, hypothalamus, anterior thalamus, cingulate cortex, association cortex and hippocampus), the prefrontal cortex, and ascending monoaminergic and cholinergic connections that innervate these areas (Gray, 1988). In contrast, the BAS is related to the functions of the mesolimbic dopaminergic system, and the

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FFS is assumed to be based on amygdala circuitry. Similar proposals have been made by other authors e.g. (Graeff, 1981), also emphasizing the role of neurochemical aspects of brain circuitry. The work of Jaak Panksepp (e.g. Panksepp, 1999) has shown that neurochemical differences and interactions between neurotransmitter systems appear to be related to coherently operating emotional systems in the brain, which he assumes to be organized in

‘basic emotions’ (Panksepp, 1999). Functional relations between brain structures as measured by means of electrophysiological methods in animals have been emphasized by Edmund T.

Rolls. Rolls’ model bears some similarity to Gray’s model in that it stresses the importance of learning theory as a framework for the understanding of emotions (Rolls, 1990).

Consequently, emotions are described in terms of their reinforcing properties rather than in terms of physiological or semantic dimensions (Rolls, 1995). Using this model, Rolls identified an emotion/learning network that includes the amygdala and orbito-frontal cortex as its key players (Rolls et al., 1980, 1996).

Several implications for the understanding of emotion follow from the theoretical approaches and empirical findings outlined so far: First, emotions are best described as multifaceted processes that must be specified on at least a behavioral and neural level.

Second, emotions cannot be understood as the consequence of functions of a single emotional brain center. Third, the most pronounced differences between qualitatively distinct emotions are to be found in the circuits of the brain that regulate emotional processes, rather than in patterns of peripheral physiological measures such as skin conductance, heart rate or body temperature.

Theories based on large scale functional data of the human brain have recently profited from new technical and methodological approaches (Cacioppo and Gardner, 1999).

Davidson’s work investigating the asymmetric organization of emotion systems in the brain has been influential in this literature, stimulating several imaging studies of brain laterality differences of emotional states (see Davidson, 1992; Davidson and Hugdahl, 1995; Davidson et al., 1999). Davidson states a version of the so-called valence hypothesis of brain asymmetries that states that approach-related processing takes place in anterior left cortices whereas withdrawal-related processing is associated with right-anterior activation (Davidson et al., 1994). Thus, the valence hypothesis holds that valence categories are represented in different hemispheric activation patterns. Davidson’s dimensional model of emotion can be extended to temperament, trait-like affective style and affective disorders (Davidson, 1998).

However, studies using modern functional imaging technology have failed to provide strong

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evidence for the assumptions stated by this theory (Cacioppo and Gardner, 1999).

In summary, the considerations outlined so far raise questions as to the mechanisms that act to relate the activity of the distributed areas involved in emotional processes to one another and finally establish emotional perception, behavior, or experience. In the following section, three contemporary models of emotional processes are presented in detail, focusing on possible substrates of such integrated processes, with an emphasis on emotional perception of external stimuli.

The LeDoux model

One of the most influential approaches to affective behavior in the field of neuroscience is the model proposed by Joseph LeDoux and his collaborators, based on work on the fear-potentiated startle reflex in rodents (see LeDoux, 1995a). Following earlier approaches, LeDoux suggests that affective phenomena fall into three categories: evaluation, expression, and experience. The focus of his work is on the neurophysiological mechanisms of affective evaluation, especially in the auditory modality. Using axonal transport tracers such as wheat-germ agglutinin conjugated horseradish peroxidase (WGA-HRP), several pathways involved in auditory fear-conditioning were identified, and the components and relations of an emotional network were outlined (see Fig I.1). According to the LeDoux model, the amygdala is the key structure of a variety of areas involved in affective phenomena (LeDoux, 1986, 1992, 1993, LeDoux et al. 1990). When a sensory stimulus is processed, amygdaloid nuclei are thought to receive inputs by way of two different routes: (1) Via the nuclei of the sensory thalamus, information on sensory events reaches sensory neocortex, higher order sensory cortices (such as the anterior inferior temporal lobe in case of the visual system) and is finally relayed to the amygdala, providing the results of high-level sensory analysis of the stimulus. (2) A fast direct connection between thalamic nuclei and lateral amygdala (dorsal archistriatum) provides the amygdala with a crude representation of the stimulus. Although these mechanisms have only been partly established, using auditory fear conditioning paradigms in the rat, LeDoux proposes that these principles may also apply for other modalities and species.

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Figure I.1: Some elements of the emotional circuitry involving the amygdala, according to the LeDoux model (adapted from LeDoux, 1993; see text for details)

The importance of the amygdala for affective evaluation is denoted by results from studies using amygdala stimulation in humans and monkeys as well as by patients suffering from selective amygdala lesions (Aggleton, 1992, 1993). In addition, previous results from conditioning experiments in rodents support the view that sensory cortex is not necessary for fear conditioning of visual stimuli, given that the CS is salient and simple in nature, e.g.

flashing lights (Doron and LeDoux, 1999; LeDoux et al., 1989). Furthermore, imaging studies in humans have shown that masked stimuli that have been associated with an unpleasant unconditioned stimulus (UCS) enhanced the effective connectivity between the superior colliculus, pulvinar, and amygdala, suggesting that thalamo-amygdaoid connections may mediate one possible route of affective evaluation that is independent of visual cortex (Morris et al., 1999).

Having received afferent information on sensory events, the amygdala is also thought to play an important role in the organization of emotional expression and experience. The efferents of the central nucleus of the amygdala, including connections to the lateral hypothalamus, central gray, dorsal vagal complex, nucleus basalis, and sensory and frontal

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cortices, allow for the regulation of a number of brain/behavioral functions according to stimulus significance. A more detailed description of amygdala efferents is given in section I.B.5. Using the above-mentioned physiological mechanisms as a starting point, LeDoux has outlined their implications for the understanding of human affective behavior and experience.

Treating emotional evaluation, expression and experience as separate processes with distinct underlying brain substrates, LeDoux proposes distinct empirical approaches for investigating these constructs. As a further consequence of this functional separation, evaluative processes are viewed as pre-conscious mechanisms that are necessary for establishing affective experience in response to external stimuli. In contrast, the emotional feeling or experience itself is considered to be conscious by definition. In summary, the LeDoux model predicts an early, fast evaluative modulation of CNS functioning in response to emotional information, as well as a later response that is the correlate of conscious stimulus processing, i.e. experience (LeDoux, 1995a). The proposal that an early differentiation between emotional states occurs before higher-level visual analysis has occurred has been criticized on the grounds that it is physiologically implausible given our current understanding of sensory processing. For example, Rolls (1995) has argued that emotional evaluation of external stimuli requires fine- grained information of the visual scene. If one accepts classical models of hierarchical visual analysis, this information is not available before visual processing reaches anterior temporal cortices. Thus, Rolls makes a strong case for a late differentiation, based on the prefrontal- amygdoloid circuitry set into motion by anterior temporal cortical structures (Rolls, 1990). As a further point, the Le Doux model’s neglect of large scale views of the nervous system must be seen as a drawback. For instance, any model of the neuronal basis of emotional perception, experinece and expression should be able to account for the large body of evidence suggesting an asymmetric organization of emotional functions in the cerebral hemispheres. proposal stressing the role of the amygdala as a center of emotional processes may be warranted given the evidence available at this time. However, lesion and electrophysiological data as well as findings from attention tha orienting research show that there may be alternative routes of processing stimulus significance in humans (see Halgren and Marinkowitch, 1995). Finally, a theory of emotion should also be stated on a psychological level in order to account for the purpose of the brain (i.e. producing adaptive behavior in an environmental context). The strength of Rolls’ and Gray‘s models, which are explicitly built upon established principles of learning, is not part of the LeDoux model. As a consequence, the relation between this neurophysiological model and findings from psychology remains unclear.

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The Damasio model

A second popular model of human emotion has been developed by Antonio Damasio and coworkers based on anatomical, neuropsychological and neuroimaging studies (see Damasio, 1994, 1998). Damasio differentiates between subjective feelings on the one hand, defined as the conscious perception of the body states associated with an emotion and, on the other hand, the emotion itself. Emotions are defined as ‘the combination of a mental evaluative process, simple or complex, with dispositional responses to that process, mostly toward the body proper, resulting in an emotional body state, but also toward the brain itself (neurotransmitter nuclei in brain stem), resulting in additonal mental changes’ (Damasio, 1994). Thus, in this view, evaluative processes are the core of the concept of emotion as well as a primary stage which is necessary for the subjective experience of one’s body state. A central role is attributed to the prefrontal cortex, which receives inputs from both sensory cortices and limbic structures, mainly the amygdala and the anterior cingulate (Damasio, 1995). According to Damasio, the prefrontal cortex integrates these signals and relates them to acquired dispositions that are associated with the perceived stimuli or the emerging subjective state. More precisely, the prefrontal cortex is thought to establish contingencies between somatic, visceral feedback and a given situation or stimulus configuration. This provides a ‘somatic marker’ that can regulate behavior according to previous experience.

Evaluation is consequently seen as a process that depends on the feedback of ‘gut feelings’.

An important contribution of this approach is the relation of bodily feedback to brain mechanisms and their consequences for emotional feelings. In this respect, the Damasio model is the only one to explain and predict two–way interactions of environmental events on the one hand, and central and peripheral changes on the other.

In terms of methodology, Damasio largely draws from lesion data obtained from neurological patients. The focus here is on a number of brain regions identified to be associated with defects in emotional behavior when lesioned (e.g. Adolphs et al., 1996). It should be emphasized that in this model stimulus evaluation is clearly suggested to be a process that is either conscious itself or preceded by conscious processes, and prefrontal activity is thought to follow at least some first steps of conscious perception and interpretation of the external stimuli. Consequently, psychophysiological measures of neuronal activity should show a late differentiation between stimuli differing in terms of emotional characteristics. In particular, a modulation at anterior recording sites would be predicted,

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reflecting differential appraisal of the information on stimulus properties and acquired dispositions. Additionally, network activity in the circuitry including prefrontal cortex, anterior cingulate, amygdalae and further structures should be associated with measurable electrocortical activity. Since Damasio emphasizes the integrated action of different brain regions, it might also be speculated as to the mechanisms being used to bring together the local processes of these distributed regions. This is a critical point, since the modular character of this model emphasizes the functional uniqueness of each part of the system. Thus, the modularity postulated in this framework presents a problem with respect to imaging and electrophysiological data, which have demonstrated evidence for parallel, complex and distributed networks rather than a sequential or modular organization of emotion (Lane et al., 1998; Liotti and Tucker, 1995). Interestingly, Damasio has proposed a model on memory and consciousness, which is based on synchronized activity of cortical ‘neuron ensembles’

(Damasio, 1989) and rejects the possibility of a single brain center that embodies functions such as recall or recognition. Using the analogy with visual processing, oscillatory brain activity might be one possible candidate to achieve this integration also in emotional processing. This point will be further discussed in section I.C.

The Lang model

The theoretical accounts of Lang and coworkers will be discussed in detail, because the present thesis adopts some important aspects of Lang's views on the relationship between emotion and attention, as well as the motivational characteristics of affective valence and arousal. Lang and coworkers have developed a system of assumptions and predictions which is often referred to as the 'bio-informational theory of emotion' (Lang et al., 1998), dealing with a number of questions that have been discussed particularly in psychophysiology.

Emotions are viewed as action dispositions, thus containing an important motivational as well as a physiological/behavioral component in addition to a cognitive component. These dispositions are organized as being either consummatory/appetitive tendencies or defensive/aversive tendencies. Consequently, this approach is associated with a two- dimensional model of emotion: The valence dimension is related to variations on the level of the two motive systems, i.e. 'appetitive' and 'aversive'. A second arousal dimension, adds to the two-dimensional affective space a component that modulates the emotional behavior with respect to activation or intensity (Lang et al., 1997). This does not imply that there will be a perfect correlation between the affective or emotional state of the organism on the one hand

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and the behavioral outcome on the other hand. This is prevented by adaptation to the situational requirements on multiple levels, external and internal, referred to as 'strategic' versus 'tactical'. Thus, although the strategic (long-term) disposition of a given organism may be defensive, the actual behavior may be shaped based on the tactical (short-term) demands of the respective situation (Lang, 1994).

The two motive systems on the valence dimension are thought to have different physiological substrates, namely widespread networks involving a number of neocortical and subcortical structures. The kind and location of these structures is discussed by Lang and coworkers in the framework of findings from neuroscientists working in the animal model (see section I.B.5). In contrast, no separate system is proposed for affective arousal.

Variations in arousal are rather considered to reflect changes in the intensity of activation in the aversive or appetitive subsystems, or the degree to which both are co-activated. An equivalent of the above-mentioned widespread neuronal networks on a descriptive level can be seen in Lang's proposal that emotions are mentally represented as propositional networks, thus containing information on a number of aspects related to affective stimuli or behaviors.

This information may also include possible reactions of the individual, as well as language and behavioral elements, information on past events or stimulus/behavior contingencies. An example of such a hypothesized propositional network with respect to snake fear is given in Fig. I.2. The view of an organization of emotions along the two dimensions of valence and arousal according to motivational principles has been the basis for a large body of research, in particular research on the human aversive motive system and its disorders, namely anxiety disorders and fear. One of the predictions of the model outlined above is that, when presented with visual stimuli, the observer's reaction can be described in terms of appetitive versus aversive behavior (valence) and degree of activation (arousal). In addition, a pre-activation of one of the valence subsystems should enhance the reaction to external stimuli, if these stimuli are of the same valence. In contrast, the reaction should be reduced when the new stimulus is of different valence as the pre-activating stimulus and thus incompatible with its behavioral disposition. This prediction has been tested extensively using the so-called 'startle response paradigm' (see Lang et al., 1990). In a typical experiment, the participant is looking at standardized affective pictures, which allow for a manipulation of the valence and intensity of affective pre-activation. When the viewer is presented with a brief, loud white noise, the startle response is elicited, a complex reflex which includes flexor activation throughout the body.

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Figure I.2: Model of a propositional network representing a snake fear episode. Adapted from Lang (1994).

The magnitude of this reflex can be assessed by measuring the eyeblink EMG at the musculus orbicularis oculi. The main finding using this paradigm in humans has been repeatedly reported from a wealth of authors: During aversive picture viewing (i.e. when the organism is in an unpleasant state) a potentiation of the startle response occurs, whereas during viewing of pleasant pictures the startle reflex is inhibited. Thus, these findings confirm the idea of independent valence subsystems which may be pre-activated and potentiate or reduce the affective response to subsequently presented stimuli, depending on the match (potentiation) or mismatch (inhibition) between affective state and type of stimulus (pleasant vs. unpleasant).

Given the important role of the affective stimuli in this paradigm, an attempt has been made to create a set of affective pictures that provides a reliable means for evoking predictable affective responses in the viewer. Lang and coworkers have published the International Affective Picture System (Lang et al., 1997), a collection of colored pictures which has normative ratings as to each pictures’ valence, arousal and dominance. In addition, a subjective rating instrument (Self-Assessment Manikin, SAM) has been developed, which allows for monitoring the self-reported affective state in a given experimental situation (Bradley and Lang, 1994). It has been shown that the reliability of the SAM is comparable with other self-report questionnaires (Bradley and Lang, 1994). Furthermore, its validity has

I-me

frightened run

alone

woods

dangerous

snake

large heart

backed

f e e l s ee w a n t

I'm afraid

eyes

quickly

am acc el er at e

s ay m ov e

i n

i s

unpredictable f o l l o w

moves i s

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been emphasized by its strong relation to other behavioral, physiological and self-report indices of an individual’s affective state (Lang et al., 1993).

The Lang model has been stimulating a huge body of empirical research since it has been published in its first form (Lang, 1979). In integrating elements from clinical psychology, neuroscience, cognitive psychology and psychophysiology it is an important step towards an account of the manifold phenomena related to human emotions. However, it has a strong focus on the emotional processes that are embodied in networks sensitive for visual stimulation. Although the principles of startle modulation and motivated attention have also been shown in the acustic modality see (Lang et al., 1998), affective fluctuations that are due to peripheral feedback, such as described in the Damasio model are underrepresented here.

Furthermore, the fact that the microstructure of cortical networks distinguishes between emotions differing in valence cannot explain the amassing evidence for an asymmetric organization of emotional processes in the brain. This point requires further specification and extension, maybe building upon cortical network models of learning or spatial selective attention, such as proposed by Desimone (1996) or Corbetta (1998).

Taken together, the theoretical accounts presented so far have converged to emphasize the network character of emotions. They differ in that they explicitly include psychological learning theory as a framework on a behavioral level, such as the Lang or the Rolls model, or rather use learning paradigms as an experimental technique such as the model of LeDoux.

Likewise, the models stress different aspects of emotion, depending on data base, methodology or theoretical and professional background of the author. This diversity affects also the matter of definition. Obviously, it is necessary to define emotion on a variety of levels, including the behavioral, the neural, the cognitive level, as was suggested by Gray.

These levels must then be related to a semantic framework. It turns out that one possible framework is the motivational or learning aspect of emotional stimuli. That is, emotional stimuli differ in their value as a primary or secondary reinforcer, having distinct effects on the individual’s motivational state. From this starting point, it is possible to explore the specific neural mechanisms associated with such distinct motivational states. Knowledge on these mechanisms can in turn clarify the functional relationship between motivational states and their behavioral organization. A further distinction can be made in terms of the time course of steps that follow the presentation of a significant stimulus. This temporal aspect of stimulus processing has been illustrated in detail by LeDoux for the neural level of emotions. It seems reasonable to accept this aspect of a spatio-temporal differentiation of the neural processes

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involved in emotional processing, because it is consistent with our understanding of the organization of the human perceptual system (Mesulam, 1998). In summary, the models outlined so far provide a theoretical framework for the present thesis by shedding light on the different aspects of emotional stimulus processing and the mechanisms that may be involved.

Consequently, a working definition for affective stimulus evaluation can be derived.

2. Affective stimulus evaluation: A working definition

On the basis of the considerations discussed above, we characterize affect or emotion as a group of multifaceted cognitive, behavioral and physiological processes in response to external or internal stimuli that have multiple levels of manifestation and a characteristic time course. These are distinguished from other processes by their connection to the individual’s motivational system. Consequently, in the case of external stimulation, affective stimulus evaluation constitutes a first necessary step in the affect system consisting of many parallel and sequential sub-processes. However, here it is assumed that visual stimulus evaluation is not limited to the first stages of visual analysis but occurs at multiple stages of perception. In summary, the present investigation implies that affective evaluation of visual external stimuli refers to the specific sub-processes that relate the emerging percept to distinct motivational states of the organism. These states may be due to innate dispositions or learned contingencies. In this respect, it is acknowledged that attentional and motivational/emotional processes are strongly connected and perhaps overlap to a large extent.

Affective evaluation of visual stimuli: empirical findings 1. Evidence from neuroimaging studies

Functional measures of cerebral blood flow or metabolism such as Positron-Emission Tomography (PET) or functional Magnet Resonance Tomography (fMRI) are especially suited for in-vivo identification of the neuroanatomical substrates involved in emotional perception. For most experimental designs, these techniques provide better spatial resolution than electrophysiological recording techniques, but have a poor temporal resolution, because they are sensitive to relatively slow metabolic changes. Using this technology, a number of investigations showed that several regions of the human brain are specifically activated when affective visual input is processed. The findings from those neuroimaging studies of emotional visual stimulus processing that are published in journals being indexed in widely

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used literature databases (i.e. Medline, PsychLit, Psychinfo) are presented in Table I.B.1. It appears that various structures that may form an affective network have repeatedly been reported as being activated during visual affective processing. For instance, these structures include the bilateral amygdala, the anterior cingulate, several areas in prefrontal cortex, the pulvinar and the visual cortices. However, to date, these findings show little convergence with respect to the regions identified to be specific for affective perception. For example, there is substantial discord as to which brain areas be specific to pleasant vs. unpleasant emotional states. Furthermore, it remains controversial whether there is a lateralization of emotional systems in general or a lateralization according to the content or valence of emotions (Lane et al., 1997c; Davidson, 1999; Liotti and Tucker, 1995). Unfortunately, many experimental paradigms do not allow for an assessment of the effects of confounded factors such as perceptual processes or spatial selective attention. Several aspects of requirements to experimental designs and their respective impact on interpretability of results are reviewed by Davidson (Davidson, 1999).

One of the most interesting findings in neuroimaging for the issue of the present thesis comes from a study conducted by Lang and coworkers (1998). Using fMRI, they observed that emotionally arousing IAPS pictures were associated with enhanced blood flow in visual cortex, as compared to calm pictures. Besides activation of right fusiform gyrus and the right inferior and superior parietal lobules, they reported bilateral activity in the occipital gyrus.

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Table I.1 : synopsis of neuroimaging studies of visual affective stimulus evaluation. Please note that studies aiming at examining facial affect recognition in other individuals are not included here, unless faces were presented to evoke emotions in the participant. ‘Control’ denotes the reference category for changes due to affect manipulation.

Authors/year/journal Method Partici- pants

Stimuli pleasant neutral unpleasant

Beauregard et al. (1998) Neuroreport

fMRI 7 controls Film clips --- not tested --- Control medial and inferior prefrontal

cortices, right middle temporal cortex, cerebellum and caudate Bremner (1999)

Biol Psychiatry

PET 10

Veterans without

PTSD

Combat scenes (pictures+sound)

--- not tested --- Control anterior cingulate (area 24)

posterior cingulate (area 23), precentral cortex, inferior parietal cortex, lingual gyrus.

Canli et al. (1998) Neuroreport

fMRI 14

females

IAPS pictures Left middle frontal gyrus, middle and superior temporal gyrus

Not tested Right inferior frontal gyrus

Dolan et al. (1996) Neuroimage

PET 12 Affective faces left ventral prefrontal cortex, left anterior cingulate cortex, right fusiform gyrus

Control --- not tested ---

George et al. (1995) Am J Psychiatry

PET 11

females

Affective faces + Recall of life events

Reduction in right prefrontal and bilateral temporal-parietal cortex

Control bilateral cingulate, medial prefrontal, and mesial temporal cortex, brainstem, thalamus, caudate, putamen.

Lane at al. (1997a) Neuroreport

PET 10

males

IAPS pictures rostral anterior cingulate (BA 32) parieto-occipital cortex (bilateral)

rostral anterior cingulate (BA 32)

Lane at al. (1997b) PET 12 Film clips and

recall

thalamus and medial prefrontal cortex (Brodmann's area 9)

Control thalamus and medial prefrontal cortex (Brodmann's area 9)

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Am j Psychiat females recall cortex (Brodmann's area 9) ventral mesial frontal cortex

cortex (Brodmann's area 9) anterior insula

Lane et al. (1997c) Neuropsychologia

PET 12

females

IAPS pictures medial prefrontal cortex thalamus, hypothalamus and

midbrain

head of the left caudate nucleus

Control medial prefrontal cortex thalamus, hypothalamus and midbrain

bilateral occipito-temporal cortex and cerebellum, and left

parahippocampal gyrus, hippocampus and amygdala Lane et al. (1998)

J Cog Neurosc

PET 12

females

Film clips and recall

Brodmann's area 24 of the anterior cingulate cortex (ACC)

Control Brodmann's area 24 of the anterior cingulate cortex (ACC)

Lang et al. (1998) Psychophysiology

fMRI 20

(8 fem.)

IAPS pictures Sulcus calcarinus Occiptal gyrus Gyrus fusiformis

Inf.and sup. parietal lobulus

Sulcus calcarinus Sulcus calcarinus Occiptal gyrus Gyrus fusiformis

Inf.and sup. parietal lobulus Morris et al (1999)

PNAS USA

PET (connectivity)

10 males

Masked conditioned emo-tional faces

--- not tested --- --- not tested --- right amygdala, pulvinar, superior colliculus

Paradiso et al (1997) Am J Psychiatry

PET 8

elderly

Film clips Limbic structures Primary and

secondary visual cortex

Limbic structures

Reiman et al. (1997) Am J Psychiatry

PET 12

females

Film clips (happy, sad, disgusting)

medial prefrontal cortex and thalamus

occipitotemporoparietal cortex, lateral cerebellum, hypothalamus, anterior temporal cortex,

amygdala, and hippocampal

Control medial prefrontal cortex and thalamus

occipitotemporoparietal cortex, lateral cerebellum, hypothalamus, anterior temporal cortex, amygdala, and hippocampal formation

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amygdala, and hippocampal formation

and hippocampal formation anterior insular cortex Schneider et al (1994)

Psychiatry Res

PET 12

(7 fem)

Happy and sad faces

Cortical decrease --- not tested --- occipital temporal region, left frontal pole

Schneider et al. (1995) Psychiatry Res

PET 16

(5 fem)

Happy and sad faces

Decrease in left amygdala Increase posterior cingulate

--- not tested --- Left amygdala increase

Schneider et al. (1997) Psychiatry Res

fMRI 12

(5 fem)

Happy and sad faces

Left amygdala --- not tested --- Left amygdala

Teasdale et al (1999) Am J Psychiatry

fMRI 6

(3 fem)

Images with affective captions

right and left insula, right inferior frontal gyrus, left splenium, left

precuneus

right and left medial frontal gyri, right anterior cingulate gyrus, right precentral gyrus, and left caudate

Control right medial and middle frontal gyri, right anterior cingulate gyrus,

right thalamus

Taylor et al (1998) Neuroimage

PET 10 Affective pictures Left amygdala Control Left amygdala

Whalen et al (1998) J Neurosci

fMRI 10 Masked faces Bilateral amygdala --- not tested --- no bilateral amygdala activation

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In terms of subcortical regions, Lane and coworkers (Lane et al., 1997c) demonstrated increase of regional cerebral blood flow in the left parahippocampal gyrus, hippocampus and amygdala using PET. This effect was most pronounced when subjects viewed unpleasant IAPS pictures. Further imaging studies are listed in Table I.B.1, showing authors, measures, stimuli and kind of respective effects. As of today, the findings obtained by functional neuroimaging may allow only a limited number of conclusions: first, besides visual cortices, a number of subcortical structures seem to be involved in affective picture processing. Second, the bilateral amygdala and the anterior cingulate appear to be important parts of the network that is active during affective evaluation. The contribution of these structures thus seems to be sufficiently extended in time, allowing a detection by neuroimaging techiques with slow temporal resolution. However, it may well be the case that these structures receive modulatory afferent information from a variety of further areas that is encoded by a firing pattern displaying limited temporal duration. Third, a clear pattern of hemisphere specialization for different emotions (valence hypothesis) or for emotional versus neutral perception (right hemisphere hypothesis, see section below) cannot be derived from the data available at this point. This lack of convergence may be due to methodological problems of the studies conducted so far. For example, several studies did not use neutral control conditions to control for unspecific effects of the experimental situation per se. In addition, the brain structures to be examined, i.e. the regions of interest for evaluation of imaging results differed between studies, depending on the authors’ theoretical orientation and study goals (Davidson, 1999).

2. Evidence from neuropsychological studies

Impairment of affective perception, experience and expression after brain lesions has been attracting the interest of investigators since the beginnings of research in brain-lesioned patients.

For example, one of the classic cases in neuropsychology, Phineas Gage, has been described as suffering especially from affective impairments associated with his frontal lobe lesion (Damasio et al., 1994). For the purpose of review, the literature on effects of brain damage on emotions can be divided in two categories (1) clinical studies, that focus on the effects of brain lesions on the patients’ behavior in daily life and (2) experimental approaches, implementing procedures from general and experimental psychology in clinical populations.

The main issue in clinical studies has been the question whether circumscribed lesions of given structures differentially affect emotional behavior in humans. In general, this work has shown that damage to the brain in a number of sites may affect emotional perception, expression,

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and experience. Based on early observations and animal studies, patients with amygdala lesions have been a target group for testing lesion-behavior relations (Aggleton, 1992). However, most types of damage to the human brain, including dystrophic illness, accidents or stroke, are usually not limited to the amygdaloid complex. In addition, the amygdala can functionally be subdivided into a number of nuclei showing vast differences in morphology and connectivity (Gray, 1999).

Accordingly, the few neurological cases displaying circumscribed lesions in the amygdala showed pronounced affective impairment as well as a number of further cognitive and behavioral problems, including learning and memory dysfunction (Aggleton, 1993). Repeatedly, lesions of the amygdala have been described to be associated with impairment of emotional perception, namely appraisal of danger and experience of fear or anger (Scott et al. 1997; Aggleton 1992), as well as expression of emotional states (Tranel and Hyman, 1990). Even when memory dysfunction was the focus of such studies, the authors emphasized the strong impact of impaired emotional behavior on the patients’ daily life (Markowitsch et al., 1994). In addition, classical cases of memory dysfunction after medial temporal lobe removal, such as HM, are described to show problems in ‘reporting and regulating internal states’ (Hebben et al., 1985). However, it remains unclear whether these phenomena result from damage to the amygdala alone or rather from lesions in nearby structures that are as well part of the relevant network.

A second focus in clinical studies has been the impact of lesions in prefrontal cortex on emotional behavior (Kolb and Taylor, 1981). Consistent findings support the notion that prefrontal cortex might be important for regulation and organization of emotional experience and behavior e.g. (Brazzelli et al., 1994). A number of case reports draw from the Damasio model of prefrontal functioning in emotion (Damasio, 1995), showing that the experience of emotional feelings as well as the expression of emotions is impaired in prefrontal patients. A major difference to individuals with amygdala lesions is seen in the fact that the former do not respond to external stimulus configurations representing reward/punishment systems (Damasio, 1994). As a consequence, these reports present important insights into brain structures necessary for emotional processing: Structures such as the amygdaloid nuclei and areas in prefrontal cortex seem to play an important role in many manifestations of emotion, including expressive behavior and emotional experience. It must be kept in mind, though, that it remains unclear whether this indicates a causal relationship between the structures named above and emotional functioning, because the data are only correlative in nature.

Experimental studies with brain-lesioned patients have taken profit from recent developments in affective psychology. Standardized stimulus material and large control groups have provided an excellent framework for the interpretation of findings obtained with patients.

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For example, (Adolphs et al., 1996) have identified a number of cortical structures that are involved in facial emotion recognition, conducting MRI based lesion analysis in a sample of 37 patients with focal brain damage. The lesions that most strongly interfered with the affect recognition task were located on the right hemisphere, i.e. the right inferior parietal cortex and the right mesial anterior infracalcarine cortex. As a further example, the startle paradigm described above was used to examine the defensive reflex modulation in patients with selective lesions of the amygdala. In one patient with right-hemisphere amygdala lesion, Angrili and coworkers (1996) found reduced startle response amplitude as compared with matched healthy control subjects. In addition, the patient did not show a pattern of startle potentiation when affective pictures were presented during application of the startle stimulus. The authors conclude that the amygdala plays a central part in mediating contralateral startle response. Furthermore, they emphasize the role of the right amygdala for the organization of aversive reactions. Tranel and coworkers used skin conductance measures in different patient groups in order to disentangle the functional role of amygdala and prefrontal cortical areas in affective evaluation. They demonstrated that skin conductance responses to emotive visual stimuli were abundant in amygdala patients (Tranel and Damasio, 1989), but not in prefrontal patients (Bechara et al., 1996). Thus, the modulation of autonomic responses to emotive stimuli seems to be mediated via the prefrontal system rather than via amygdala circuitry (see also Zahn et al., 1999).

Regarding functional brain asymmetries, some evidence is available that right-hemisphere lesions are related to more dramatic changes in affective behavior (Borod et al., 1996), and perception (Borod et al., 1992), which led to the assumption that emotions are primarily generated in the right hemisphere, known as the right hemisphere hypothesis, whereas the left hemisphere is involved in ‘rational’ or ‘abstract’ processing. Although this hypothesis still prevails in some of the contemporary literature, it has been extended and improved by taking into account the precise location of lesions, the nature of the stimuli evoking an emotion, and the differences between affective perception and affective behavior (Zahn et al., 1999; Kolb and Taylor, 1981). For example, recent work on asymmetries in facial expressions found that support for the valence hypothesis or right-hemisphere hypothesis depended on the measure used for emotional state. More precisely, self-report measures of emotional state were associated with support for the valence hypothesis, whereas observer judgements and EMG quantification in the same set of data resulted in support for the right-hemisphere hypothesis (Borod et al., 1998).

Reviewing the literature, Silberman and Weingartner (1986) conclude that ‘the present level of knowledge suggests a model of emotional control based on interactive inhibition between a right negatively biased and left positively biased hemisphere. However, the details of such a model,

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including the precise conditions under which emotion-related functions are lateralized, and the mechanisms of such lateralization have yet to be elucidated.’ This brief review of findings from experimental neuropsychology supports the last phrase of this notion. Obviously, there are many results such as the findings from (Adolphs et al., 1996) or Borod, (Borod, 1992; Borod et al. 1992, 1993, 1996, 1998) that are better in accord with the right-hemisphere hypothesis.

Additionally, the exact experimental task and stimulus type seems to be a critical factor in predicting experimental outcome regarding lateralization. Thus, the question of lateralization requires a multivariate approach, using additional measures and experimental tasks in order to specify the conditions under which hemisphere asymmetries occur.

3. Evidence from ERPs / event-related magnetic fields

Only a limited number of studies have examined the effects of visual stimuli differing in affective valence and arousal for the ERP recorded in human volunteers (see Cacioppo and Gardner, 1999, for review). Meanwhile, several studies using standardized IAPS pictures have converged, showing a late positivity beginning in the time range of about 300 ms after onset of a visual stimulus (Mini et al., 1996; Palomba et al., 1997; Diedrich et al., 1997). This positivity has been reported to be more pronounced during presentation of affectively arousing pictures, compared with neutral or calm IAPS slides. However, enhanced P300 or slow potential ERP components have also been reported in response to other stimulus material differing in arousal from control stimuli (Laurian et al., 1991; Carretie et al., 1997). Although there is considerable consistence across studies as to the time course of the effect, there is still discord as to whether this ERP modulation originates from visual cortices or from frontal sources. Accordingly, the differences might reflect enhanced visual processing of the affective pictures (Lang et al., 1997) or inhibition of emotional responses in the lab situation (Diedrich et al., 1997). Recent findings from studies using source localization and high-density EEG arrays support the view that slow potential modulation is generated by higher order visual cortices (Junghöfer et al., 1999). This does not exclude possible top-down influence from frontal networks. In an extension of these findings, Ito and collaborators (1998) replicated the result of a late positive wave modulation as a function of arousal and showed that amplitude enhancement was higher for unpleasant than pleasant pictures. These authors have interpreted their finding as supportive for a negativity bias in affective perception (Cacioppo and Gardner, 1999).

In addition, several authors report lateralization of ERPs in response to arousing pictures to the right hemisphere (Laurian et al., 1991; Roschmann and Wittling, 1992). Most interestingly, (Kayser et al., 1997) found evidence for asymmetric ERP topographies in a hemifield paradigm.

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An effect of emotional content on ERP components N2, early P3, late P3, and slow wave was observed. Asymmetries were seen for N2 and early P3, with maximal effects over the right parietal region. N2-P3 amplitude was augmented for negative and reduced for neutral stimuli over right hemisphere regions.

One drawback of these studies, however, is the limited number of electrodes and the lack of spatial deblurring or source estimation techniques. In the present thesis, a high density electrode array was used as well as a data analysis procedure (minimum norm estimate, MNE;

(Hämäläinen and Ilmoniemi, 1984) allowing for an estimation of the cortical sources of the transcranially measured event-related potential. This approach was considered to shed light on questions as to the source configuration of the late positive wave and its modulation.

Furthermore, the time-locked activation of cortical areas can be exactly examined also during earlier time windows. The latter aspect has been neglected in most previous work, since the focus was on correlates of emotional experience, which are assumed to manifest themselves in late ERP windows (Mini et al., 1996). This assumption seems to be no longer justified, given the findings from animal literature that suggest a fast evaluation mechanism (LeDoux, 1995a, 1995b).

MEG technology is only at the beginning of being used as a means for examining affective processing in humans. To date, two studies have been published examining emotional modulation of event-related magnetic fields. Streit and coworkers (Streit et al., 1999) examined the time course of brain activation during a facial emotion recognition task. They reported activation in inferior frontal cortex, amygdala and different parts of temporal cortex in response to affective faces that was organized in a consistent temporal sequence. It is however questionable whether amygdala activity can be assessed using MEG (George et al., 1995; Hari and Lounasmaa, 1989). Surakka et al. (1998) tested the mismatch negativity (MMN) during text reading, pleasant, neutral and negative slide viewing. They found that the MMN was significantly attenuated during viewing pleasant slides as compared to other conditions. The authors conclude that extremely pleasant stimulation reduces the need for auditory change detection. This finding shows that even intermodally induced emotion can modulate cortical responses as early as 180 ms post stimulus, where the MMN was beginning in this experiment. Thus, MEG is a promising tool for investigating into cortical activity during affective perception. Given its high temporal and spatial accuracy, as well as sensitivity to tangential dipoles (Murro et al., 1995), it constitutes a complementary methodology to EEG/ERP studies.

4. Evidence from EEG frequency measures and EEG asymmetry

A large part of the work on EEG asymmetries, mostly using the EEG alpha band (i.e. 8-12

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Hz) has been inspired by the proposal that the cerebral hemispheres contribute differentially to human emotionality. The most popular approach in this context has been proposed by Richard J.

Davidson and coworkers. Davidson suggests that emotional states can be expressed in terms of approach or withdrawal tendencies. Each of these dimensions possesses a physiological substrate in anterior cortical areas: positive affect is assumed to be processed by the left hemisphere, whereas negative affect is predominantly processed by the right hemisphere (Davidson, 1995).

These central assumptions are based on data from EEG asymmetry studies with healthy participants, showing that individual differences in approach- and withdrawal-related emotional reactivity and temperament are associated with stable differences in baseline measures of activation asymmetry in these anterior regions. In these studies, ‘activation’ is usually operationalized as a relative decrease in the EEG alpha (8-12 Hz) frequency band (Davidson, 1988). This however is questionable since alpha enhancement has also been reported in cognitive and perceptual tasks (Schürmann and Basar, 1994; Schürmann et al., 1997). Phasic alpha asymmetries according to Davidson’s hypothesis have been observed in response to visual emotive stimuli such as emotional pictures or film clips (Davidson et al., 1990). Furthermore, studies with depressed participants have been conducted, demonstrating that patients’ EEG spectra showed greater alpha power (Davidson et al., 1985) at the left hemisphere as compared to the right. Retest-reliability of these parameters has been reported to be as high as between 0.66 and 0.73. Although these results have been replicated several times by the original authors (Davidson, 1998) and other groups (Wiedemann et al., 1999), some attempts to replicate the findings failed (Meyers and Smith, 1986), and the reliability of the procedure has been questioned (Collet and Duclaux, 1987). Furthermore, methodological questions have been raised as to the role of the electrode reference, the filtering and averaging procedure (Davidson, 1998). In addition, changes in the subjects’ attitude towards the experiment have been shown to reverse laterality effects in a re-test session (Schulter and Papousek, 1999), which questions their use as a temperament trait marker as proposed for instance by Davidson et al. (1994).

Besides these findings, other authors have focused on the relationship between emotional processing and EEG frequency measures other than alpha power. For example, in a classical study, Ray and Cole (1985) reported higher beta activity (16-24 Hz) in right hemisphere temporal and parietal areas, whereas the alpha band showed no variation as a function of emotional processing. Furthermore, Aftanas and co-workers (1998) have found that their measure for non- linear dynamical coupling of different brain areas distinguished between positive and negative valence for higher frequencies (up to 28 Hz) but not for the alpha band. In a study of high- frequency brain activity in emotional processing, De Pascalis et al. (1987) showed a relationship

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between lateralization of 40-Hz EEG and emotional processing in a sample of hypnotizable subjects. 40-Hz spectral power was increased over both left and right hemispheres during positive emotional tasks, whereas activity over the left decreased and activity over the right hemisphere increased during negative emotional tasks. It may therefore well be that high-frequency responses can be used as a correlate of emotional processes.

5. Evidence from animal studies

The role of the amygdala and adjacent structures in the medial temporal lobe has been one focus of animal research in emotional behavior. Early studies reported the occurrence of the Klüver-Bucy syndrome after removal of temporal lobe structures in primates. The Klüver-Bucy syndrome includes behavioral features such as hypersexuality, reduction of fear responses and pica (Klüver and Bucy, 1937). In a vast number of subsequent studies, the role of the respective structures in medial temporal lobe for this cluster of behaviors was investigated using lesion techniques in monkeys (see Weisskrantz, (1956), for review). As a main result, the importance of the amygdala in establishing stimulus-response contingencies was demonstrated. In addition to learning impairments, monkeys with specific amygdala lesions have been described to display (1)

‘increased tameness and lessening or disappearance of previously acquired fear responses, (2) more rapid extinction of conditioned avoidance, the response having been established preoperatively, (3) no differences in retention of avoidance behavior, but a slower acquisition rate which they shared with the temporal control animals’ (Weiskrantz, 1956). Contemporary animal work has put less emphasis on this element of amygdala functioning, but stressed the amygdala’s part in mediating defensive reflexes in response to aversive stimuli.

Table I.2. Amygdala efferents, based on Amaral et al., (1992) and LeDoux, (1993).

Target structure Possible function

Lateral hypothalamus Modulation of autonomic functioning

Central Gray Behavioral manifestation of arousal level

Dorsal vagal complex (dorsal motor nucleus and nucleus tractus solitarii)

Control of visceral functions, indirect modulation of noradrenaline release in the forebrain

Nucleus basalis Meynert Modulation of arousal via the ascending ACH projections to forebrain

Sensory cortices Modulation of sensory processing

Orbital prefrontal cortex Modulation of contingency learning / working memory Hippocampus Modulation of explicit and implicit emotional memories Anterior cingulate Modulation of attention and long term memory encoding

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The fear-potentiated startle paradigm in rodents has led to amass evidence for a differential involvement of amygdaloid nuclei, central gray, lateral lemniscus and nucleus reticularis pontis caudalis (Walker et al., 1997; Rosen et al., 1991; Rosen and Davis, 1990; Boulis and Davis, 1989; Tischler and Davis, 1983). Table I.2 shows some of the most important afferents of the primate amygdala’s basal/central nucleus and their possible functions.

Figure I.3: Functional organization of the connections between amygdala and visual cortex; A:

projections from the amygdala reach visual areas on all levels of processing including occipital (OC), anterior occipital (OA), and temporal occipital (TEO) cortex, but direct afferent information originates in high-level temporal areas (TE) only. B: within amygdala circuitry; fibers reach the amygdala via the lateral nucleus (L) and efferents to visual cortex leave via the basal nucleus (B). Adapted from Amaral et al., (1992).

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It is evident that the amygdala by its own is not capable of emerging emotions or evaluating stimuli for their emotional significance. Rather, it is the key site in a network that is capable to quickly adapt to changes in environmental demands and organize the biological functioning of the organism according to these demands. For the present thesis, the projections from the basal nucleus of the amygdala to visual cortices deserve more precise discussion. It is clear from neuroanatomical work that the amygdala does not receive direct input from primary or secondary visual cortex. Rather, it receives fibers from visual areas at the highest level of hierarchy such as area TE (Amaral et al., 1992). In contrast, the amygdala has strong efferent connections with all levels of visual cortex, projecting both to striate cortex and higher areas.

This fact is illustrated in Figure I.3. Consequently, an affective modulation of visual processing might be expected at several stages: In an early stage, the visual input might be roughly evaluated in the amygdala via fast fibers originating in the Thalamus, which do not provide fine grained information, but a coarse representation. A second stage of evaluation via the amygdaloid complex would be much more delayed and would follow high-level visual processing, thus being based on detailed representation of the visual scene.

C. Oscillatory activity in the brain: Theoretical issues and functional correlates

1. Gamma-band activity (GBA)

Gamma-band activity refers to those oscillations in electrophysiological recordings that lie in the higher frequency range of the temporal spectrum, typically above 20 Hz. A useful approach for a classification of the brain’s oscillatory activity is the frequently cited nomenclature introduced by Galambos (1992). Galambos distinguished between (1) Spontaneous gamma rhythms, which are not related to any stimulus, (2) Evoked gamma band responses, which are elicited and precisely time-locked to the onset of an external stimulus, (3) Emitted gamma band oscillations, which are time-locked to a stimulus that has been omitted, and (4) induced gamma band rhythms that are initiated by but not time- and phase-locked to a stimulus. In the present thesis, we will focus on the latter phenomenon as well as on the steady-state visual evoked potential (see section I.C.2), which can be regarded as a special case of evoked oscillatory activity (Tallon-Baudry and Bertrand, 1999), in that the spectral characteristics of SSVEP are mainly determined by the frequency of the external driving stimulus.

Although most of the pioneering work in the field of induced oscillations has been

Oscillatory Brain Activity in Human Affective Stimulus Processing