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Effects of electrical stimulation of the amygdaloid central nucleus on neocortical arousal in the rabbit
Abstract
This study sought to determine whether electrical stimulation of the amygdaloid central nucleus (ACe) produces cholinergically mediated neocortical arousal manifested in the suppression of frontal cortex delta wave (1-4 Hz) activity. Stimulation in both anesthetized and conscious rabbits produced a suppression of delta activity that was accompanied by bradycardia and blocked by cholinergic antagonists. Stimulation of the adjacent putamen did not produce delta suppression, whereas stimulation of the adjacent ventral globus pallidus produced a suppression of shorter duration than that produced by ACe stimulation. The results suggest that the ACe influences neocortical arousal, which may be mediated by its influence on the activity of cholinergic neurons of the nucleus basalis.
... For example, studies in adults have shown that the heart rate deceleration response is augmented when the subject is viewing unpleasant scenes or angry facial expressions (Bradley, Lang, & Cuthbert, 1993;Kolassa & Miltner, 2006). Also, the neural systems that are involved in processing facial expressions of emotions (i.e., the amygdala) are closely linked with those subcortical systems that control heart rate deceleration (Kapp, Supple, & Whalen, 1994). ...
... In studies with adults, the deceleration phase of the heart rate change scores has typically not been analyzed separately for emotion effects, but inspection of the figures published in the context of these studies shows that the larger heart rate response to emotionally negative stimuli arises during the first 500 or 1000 ms of stimulus viewing (Bradley et al., 1993;Kolassa & Miltner, 2006). The surface similarity of the initial part of the infants' and adults' deceleration response suggests that a common (possibly amygdala-centered) neural network may mediate this effect (Kapp et al., 1994). Bradley (2009) drew a parallel between the enhanced cardiac orienting response in humans and the slowing of the heart rate in the context of threatening cues in animals (i.e., bradycardia), and noted that the cardiac deceleration may be part of a defense-related orienting reflex that acts to facilitate perceptual processing and extraction of information about potentially significant stimuli. ...
... A similar dissociation of the orienting mechanisms and more voluntary attentional mechanisms is suggested by previous findings showing that the orienting phase of attention is attenuated (i.e., shortened in duration) and the more voluntary sustained attention phase enhanced (i.e., prolonged in duration) when infants are presented with interesting dynamic stimuli (Courage et al., 2006). Although brain activity was not measured in the present study, it is interesting to speculate on the basis of previous work that the enhanced initial orienting response to fearful expressions may reflect a relatively automatic response that is mediated by subcortical systems involved in heart rate control (Kapp et al., 1994), whereas the effects of fearful facial expressions on saccadic eye movements may involve more voluntary attention regulation processes, possibly mediated by connections between the amygdala and eye movement control circuits in the prefrontal cortex (Johnson, 2005;Munoz & Everling, 2004;Pessoa, 2009). ...
To examine the ontogeny of emotion—attention interactions, we investigated whether infants exhibit adult-like biases in automatic and voluntary attentional processes towards fearful facial expressions. Heart rate and saccadic eye movements were measured from 7-month-old infants (n = 42) while viewing non-face control stimuli, and neutral, happy, and fearful facial expressions flanked after 1000 ms by a peripheral distractor. Relative to neutral and happy expressions, fearful expressions resulted in a greater cardiac deceleration response during the first 1000 ms of face-viewing and in a relatively long-lasting suppression of face-to-distractor saccades. The results suggest that the neural architecture for the integration of emotional significance with automatic attentional orienting as well as more voluntary attentional prioritization processes is present early in life.
... Studies of the non-human animal amygdala have shown that sensory information received by the BLA is then passed to the Ce [45]. Though outputs exist at the level of the BLA, a majority of outputs originate from the Ce [46]. The Ce projects directly to the hypothalamus and brain stem nuclei that drive autonomic and somatomotor responding [47]. ...
... The Ce projects directly to the hypothalamus and brain stem nuclei that drive autonomic and somatomotor responding [47]. The Ce also projects to all major neuromodulatory systems including dopaminergic, cholinergic, serotonergic and noradrenergic systems [46]. Thus, while direct projections can primarily affect physiological and motor responses, these neuromodulatory projections can serve to globally, nonspecifically and instantaneously effect neuronal excitability across the brain. ...
... Thus, while direct projections can primarily affect physiological and motor responses, these neuromodulatory projections can serve to globally, nonspecifically and instantaneously effect neuronal excitability across the brain. Such changes could serve to induce a state of heightened vigilance rendering the organism a more efficient consumer of information in biologically relevant learning situations [46]. One such situation involves the acquisition and expression of learned responses through classical conditioning [48,49]. ...
The dynamic interactions between the amygdala and the medial prefrontal cortex (mPFC) are usefully conceptualized as a circuit that both allows us to react automatically to biologically relevant predictive stimuli as well as regulate these reactions when the situation calls for it. In this review, we will begin by discussing the role of this amygdala-mPFC circuitry in the conditioning and extinction of aversive learning in animals. We will then relate these data to emotional regulation paradigms in humans. Finally, we will consider how these processes are compromised in normal and pathological anxiety. We conclude that the capacity for efficient crosstalk between the amygdala and the mPFC, which is represented as the strength of the amygdala-mPFC circuitry, is crucial to beneficial outcomes in terms of reported anxiety.
... Duffy, 1941;Lindsley, 1951;Schachter and Singer, 1962;Schachter, 1975;Schildkraut and Kety, 1967;Mandler, 1975;Lang, 1994;Robbins, 1997) and is also important in contemporary dimensional theories of emotion (Russell, 1980(Russell, , 2003Russell and Barrett, 1999) and some neural models of emotion (e.g. Whalen, 1998;Davis and Whalen, 2001;Gallagher and Holland, 1994;Kapp et al, 1994;Lang and Davis, 2006). However, it is important to ask how generalized arousal is triggered in emotional situations, and how the arousal, once present, affects further processing. ...
... Thus, central amygdala outputs target dendritic areas of norpeiphrine, dopamine, serotonin, and acetylcholine containing neurons and cause these to release their chemical products in widespread brain areas (e.g. Reyes et al, 2011;Gray, 1993;Weinberger, 1995;Kapp et al, 1994). Central amygdala outputs also target neurons that activate the sympathetic division of the autonomic nervous system, which releases adrenergic hormones from the adrenal medulla, and the hypothalamic-pituitaryadrenal axis, which releases cortisol from the adrenal cortex (Gray, 1993;Talarovicova et al, 2007;Loewy, 1991;Reis and LeDoux, 1987). ...
I propose a reconceptualization of key phenomena important in the study of emotion-those phenomena that reflect functions and circuits related to survival, and that are shared by humans and other animals. The approach shifts the focus from questions about whether emotions that humans consciously feel are also present in other animals, and toward questions about the extent to which circuits and corresponding functions that are present in other animals (survival circuits and functions) are also present in humans. Survival circuit functions are not causally related to emotional feelings but obviously contribute to these, at least indirectly. The survival circuit concept integrates ideas about emotion, motivation, reinforcement, and arousal in the effort to understand how organisms survive and thrive by detecting and responding to challenges and opportunities in daily life.
... By way of these connections, the neurons in the centromedial nuclei can participate in stimulus evaluation and also modulate the activity of autonomic centers to maintain a level of general vigilance. Indeed, electrical stimulation of the central nucleus increases attention and orienting (Gallagher et al., 1990;Kapp et al., 1994) by activating the cholinergic neurons in the basal forebrain. These neurons synchronize cortical activity and switch the cortex from slow oscillations to low-amplitude fast oscillations (Dringenberg and Vanderwolf, 1996) characteristic of attentive states. ...
... An alternative explanation for the higher propensity of the CM neurons to signal task events is the purported role of the amygdala in allocating attention to relevant stimuli (Kapp et al., 1994;Davis and Whalen 2001;Sander et al., 2003). Whether the fixspot-on, image-on, and image-off events acquired relevance through conditioning or these events are intrinsically relevant for the ongoing behavior, it is clear that these events require some form of attention. ...
Based on cellular architecture and connectivity, the main nuclei of the primate amygdala are divided in two clusters: basolateral (BL) and centromedial (CM). These anatomical features suggest a functional division of labor among the nuclei. The BL nuclei are thought to be involved primarily in evaluating the emotional significance or context-dependent relevance of all stimuli, including social signals such as facial expressions. The CM nuclei appear to be involved in allocating attention to stimuli of high significance and in initiating situation-appropriate autonomic responses. The goal of this study was to determine how this division of labor manifests in the response properties of neurons recorded from these two nuclear groups. We recorded the activity of 454 single neurons from identified nuclear sites in three monkeys trained to perform an image-viewing task. The task required orienting and attending to cues that predicted trial progression and viewing images with broadly varying emotional content. The two populations of neurons showed large overlaps in neurophysiological properties. We found, however, that CM neurons show higher firing and less regular spiking patterns than BL neurons. Furthermore, neurons in the CM nuclei were more likely to respond to task events (fixation, image on, image off), whereas neurons in the BL nuclei were more likely to respond selectively to the content of stimulus images. The overlap in the physiological properties of the CM and BL neurons suggest distributed processing across the nuclear groups. The differences, therefore, appear to be a processing bias rather than a hallmark of mutually exclusive functions.
... The essential idea is that associative LTP can increase the strength of the previously weak CS input (see T. H. to the extent that the CS-driven connections become sufficiently strong to generate output from the amygdala (Kapp, Whalen, Supple, & Pascoe, 1992;Lam et al., 1996;LeDoux, 1993LeDoux, , 1995Maren, 1996). This CS-generated output from the amygdala can orchestrate changes in the usual behavioral indices of conditioned fear (Aggleton, 1992;Applegate, Frysinger, Kapp, & Gallagher, 1982;Applegate, Kapp, Underwood, & McNall, 1983;Gallagher & Chiba, 1996;Gallagher, Kapp, McNall, & Pascoe, 1981;Kapp, Frysinger, Gallagher, & Haselton, 1979;Kapp, Gallagher, Underwood, McNall, & Whitehorn, 1982;Kapp, Supple, & Whalen, 1994;Lam et al., 1996;LeDoux, 1995;Maren, 1996;Scott et al., 1997;Whalen & Kapp, 1991). ...
... The increased activity in the ALa is presumed to increase the output from the ACe, which is believed to be responsible for generating certain CRs Kapp et al., 1979;Kapp et al., 1982;Kapp et al., 1994;Kapp et al., 1992;Lam et al., 1996;LeDoux, 1993LeDoux, , 1995. In accordance with the BCM rule (Figure 4), longterm synaptic depression (LTD) can, in principle, occur (Debanne, Gähwiler, & Thompson, 1994;Kirkwood, Lee, & Bear, 1995;Mulkey, Herron, & Malenka, 1993;Oliet, Malenka, & Nicoll, 1997) during nonreinforced (extinction) trials when the CS input is active but the level of post-synaptic activity is low (because there is no strong input from the US). ...
Presents a real-time model of fear conditioning in which the functional anatomy and neurophysiology of the lateral amygdala and perirhinal cortex provide a mechanism for temporal learning during Pavlovian conditioning. The model uses realistic neuronal and circuit dynamics to map time onto space and relies on a conventional Hebbian learning rule that requires strict temporal contiguity for synaptic modification. The input-output relationships of the model neurons simulate our physiological recordings with respect to latency to fire, firing frequency, and accommodation tendency. Chains of these neurons form a spectrum of activity windows delayed by various amounts from the conditioned stimulus onset. Simulations reveal that learning occurs only when the conditioned and unconditioned stimuli are explicitly paired, that the interstimulus interval (ISI) is accurately learned over a time range from 0.5 to 16 sec, and that low-frequency noise causes the accuracy of temporal learning to decrease as the ISI increases, in accordance with a Weber-type law. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
... In der vorliegenden Arbeit führten nur Salicylatinjektionen zu einer stark erhöhten Anzahl (Kapp et al., 1994;Han et al., 1999;Cain et al., 2002). In der vorliegenden Arbeit wurden Arg3. ...
... Stimuliert man die CeA elektrisch, kommt es im frontalen Cortex von Hasen zu einer Unterdrückung der "delta-wave" (1-4 kHz) Aktivität, was auf einen Anstieg des Wachheitsgrads hindeutet. Dieser Effekt kann durch cholinerge Antagonisten blockiert werden(Kapp et al., 1994). Es wurde daher vorgeschlagen, dass CeA den Erregungszustand des Cortex über die cholinergen, aus dem basalen Vorderhirn stammenden Afferenzen modulieren kann. ...
... The neural substrate for this effect seems to consist of the projections of the amygdalar central nucleus to the lateral tegmental field in the thalamus which, in turn, project to a variety of cranial motor nuclei (Hopkins & Holstege, 1978;Takeuchi, Satoda, Tashiro, Matsushima, & Uemura-Sumi, 1988). Thus, via these connections, the amygdala might modulate various reflexes, such as the nictitating membrane reflex (Whalen & Kapp, 1991;Kapp, Supple & Whalen, 1994) independently of the IPN. ...
... The projections from the amygdala to the cerebellum, then, are the crucial connection when postulating a brain mechanism responsible for the interaction of diffuse and discrete associations. Projections of the amygdalar central nucleus (ACe) to the lateral tegmental field in the thalamus, which project onto a variety of cranial motor nuclei, may form the substrate by which the ACe contributes to the conditioned modulation of various reflexes, such as the nictitating membrane reflex (Whalen & Kapp, 1991;Kapp, Supple & Whalen, 1994). ...
... Research with animals (e.g., Davis, 2000; Fanselow and Poulos, 2005; Kapp et al., 1994; LeDoux, 2003) has defined the key neural structures in this survival network (see Fig. 1: Lang and Davis, 2006; see also, Davis and Lang, 2003): The bilateralamygdalae – two small, almond shaped bundles of nuclei in the temporal lobe – plays a central role. Each amygdala receives input from cortex and thalamus (sensory) and hippocampus (memory), subsequently engaging through the central nucleus and extended amygdala (basal nucleus of the stria terminalis) a range of other brain centers that modulate sensory processing (vigilance), increase related information processing , and activate autonomic and somatic structures that mediate defensive or appetitive actions. ...
The general thesis examined here is that experienced emotions are founded on the activation of neural circuits that evolved in the mammalian brain to ensure the survival of individuals and their progeny. Primitively, these motive circuits were engaged by external stimuli that are appetitive and potentially life sustaining, or alternatively, represent threats to the organism's survival. The psychobiological consequences of this neural firing are potentially twofold: On the one hand, they engage sensory systems that increase attention and facilitate perceptual processing, and on the other, they initiate reflex responses that mobilize the organism and prompt motor action. Research with animals (e.g., Davis, 2000; Fanselow and Poulos, 2005; Kapp et al., 1994; LeDoux, 2003) has defined the key neural structures in this survival network (see Fig. 1: Lang and Davis, 2006; see also, Davis and Lang, 2003): The bilateralamygdalae – two small, almond shaped bundles of nuclei in the temporal lobe – plays a central role. Each amygdala receives input from cortex and thalamus (sensory) and hippocampus (memory), subsequently engaging through the central nucleus and extended amygdala (basal nucleus of the stria terminalis) a range of other brain centers that modulate sensory processing (vigilance), increase related information proces-sing, and activate autonomic and somatic structures that mediate defensive or appetitive actions. It is convenient to consider this survival circuit as organized into two motivational systems, one defensive and associated with reports of unpleasant affect and the other appetitive, associated with pleasant affect. Konorski (1967) early conceived such a motivational typology, keyed to the survival role of the body's many unconditioned reflexes. Exteroceptive reflexes were either preservative (e.g., ingestion, copulation, nurture of progeny) or protective (e.g., withdrawal from or rejection of noxious agents). He further suggested that affective states were consistent with this preservative/protective grouping: Preservative emotions include such affects as sexual passion, joy, and nurturance; fear and anger are protective affects. Dickinson and Dearing (1979) developed Konorski's distinction, renaming the two motivational systems, aversive and attractive, with each again activated by a different, but equally wide range of unconditioned stimuli, determining perceptual-motor patterns and the course of learning. In this general view, affective valence is determined by the dominant motive system: the appetitive system (preservative/attractive) prompts positive affect; the defense system (protective/aversive) is the source of negative affect. Affective arousal reflects the ''intensity'' of motivational mobilization, determined originally by Biological Psychology xxx (2009) xxx–xxx 1 2 3 4 5 6 7 8 Psychophysiological and neuroscience studies of emotional processing undertaken by investigators at the University of Florida Laboratory of the Center for the Study of Emotion and Attention (CSEA) are reviewed, with a focus on reflex reactions, neural structures and functional circuits that mediate emotional expression. The theoretical view shared among the investigators is that expressed emotions are founded on motivational circuits in the brain that developed early in evolutionary history to ensure the survival of individuals and their progeny. These circuits react to appetitive and aversive environmental and memorial cues, mediating appetitive and defensive reflexes that tune sensory systems and mobilize the organism for action and underly negative and positive affects. The research reviewed here assesses the reflex physiology of emotion, both autonomic and somatic, studying affects evoked in picture perception, memory imagery, and in the context of tangible reward and punishment, and using the electroencephalograph (EEG) and functional magnetic resonance imaging (fMRI), explores the brain's motivational circuits that determine human emotion.
... In humans, the anterior ventral and posterior dorsal aspects of the amygdala correspond to the lateral nucleus and the central nucleus of the amygdala, respectively (Mai et al., 1997;Whalen et al., 2001). According to anatomical data obtained in animal studies, the former is considered the major input system of the amygdala, receiving inputs from various sensory systems (Amaral et al., 1992;LeDoux, 1996), whereas the latter is considered a major output system of the amygdala, communicating with cortical systems through its connections with various neuromodulatory systems, such as the basal forebrain (Kapp et al., 1994;Jolkkonen et al., 2002). Despite the limited spatial resolution of fMRI, a similar anatomical distinction within the amygdala has been observed in a number of recent human fMRI studies, including those with resolution levels (i.e. 3 Â 3 Â 3 mm 3 voxel size) that are routinely employed by numerous neuroimaging laboratories (Morris et al., 2001;Whalen et al., 2001;Kim et al., 2003;Davis et al., 2010;Gamer et al., 2010;Bach et al., 2011). ...
Despite the well-known role of the amygdala in mediating emotional interference during tasks requiring cognitive resources, no definite conclusion has yet been reached regarding the differential roles of functionally and anatomically distinctive subcomponents of the amygdala in such processes. In the present study, we examined female participants and attempted to separate the neural processes for the detection of emotional information from those for the regulation of cognitive interference from emotional distractors by adding a temporal gap between emotional stimuli and a subsequent cognitive Stroop task. Reaction time data showed a significantly increased Stroop interference effect following emotionally negative stimuli compared to neutral stimuli, and functional magnetic resonance imaging data revealed that the anterior ventral amygdala (avAMYG) showed greater responses to negative stimuli compared to neutral stimuli. In addition, individuals who scored high in neuroticism showed greater posterior dorsal amygdala (pdAMYG) responses to incongruent compared to congruent Stroop trials following negative stimuli, but not following neutral stimuli. Taken together, the findings of this study demonstrated functionally distinctive contributions of the avAMYG and pdAMYG to the emotion-modulated Stroop interference effect and suggested that the avAMYG encodes associative values of emotional stimuli while the pdAMYG resolves cognitive interference from emotional distractors.
... The CMA plays a significant role in regulating attentional processing of cues during associative conditioning and generating emotional and associated physiological responses to threat or pain through projections to the brainstem, as well as the cortical and striatal regions 26,28 . Stimulation of the central nucleus of the AMY leads to fast, desynchronized cortical EEG activity, which is associated with increased attention and vigilance 29,43 . Projections from the central nucleus to the ventral tegmental area mediate stress-induced increases in dopamine metabolites in the prefrontal cortex 44 . ...
Altered resting-state functional connectivity (FC) of the amygdala (AMY) has been demonstrated to be implicated in schizophrenia (SZ) and attenuated psychosis syndrome (APS). Specifically, no prior work has investigated FC in individuals with APS using subregions of the AMY as seed regions of interest. The present study examined AMY subregion-based FC in individuals with APS and first-episode schizophrenia (FES) and healthy controls (HCs). The resting state FC maps of the three AMY subregions were computed and compared across the three groups. Correlation analysis was also performed to examine the relationship between the Z-values of regions showing significant group differences and symptom rating scores. Individuals with APS showed hyperconnectivity between the right centromedial AMY (CMA) and left frontal pole cortex (FPC) and between the laterobasal AMY and brain stem and right inferior lateral occipital cortex compared to HCs. Patients with FES showed hyperconnectivity between the right superficial AMY and left occipital pole cortex and between the left CMA and left thalamus compared to the APS and HCs respectively. A negative relationship was observed between the connectivity strength of the CMA with the FPC and negative-others score of the Brief Core Schema Scales in the APS group. We observed different altered FC with subregions of the AMY in individuals with APS and FES compared to HCs. These results shed light on the pathogenetic mechanisms underpinning the development of APS and SZ.
... We suggest that, rather than attending more during emotional events, individuals are attending differently, with less reliance on effortful attentional and executive processes to enhance encoding and memory. These emotional modulatory interactions [e.g., (Kapp et al., 1994)] may generate a unique aura of salience that influences the subjective experience of perceptual vividness in the moment (Berridge, 2003). ...
Highly emotional events are associated with vivid "flashbulb" memories. Here we examine whether the flashbulb metaphor characterizes a previously unknown emotion-enhanced vividness (EEV) during initial perceptual experience. Using a magnitude estimation procedure, human observers estimated the relative magnitude of visual noise overlaid on scenes. After controlling for computational metrics of objective visual salience, emotional salience was associated with decreased noise, or heightened perceptual vividness, demonstrating EEV, which predicted later memory vividness. Event-related potentials revealed a posterior P2 component at ∼200 ms that was associated with both increased emotional salience and decreased objective noise levels, consistent with EEV. Blood oxygenation level-dependent response in the lateral occipital complex (LOC), insula, and amygdala predicted online EEV. The LOC and insula represented complimentary influences on EEV, with the amygdala statistically mediating both. These findings indicate that the metaphorical vivid light surrounding emotional memories is embodied directly in perceptual cortices during initial experience, supported by cortico-limbic interactions.
... The laterobasal nuclei group is believed to send its highly preprocessed information mostly towards the centromedial group, the amygdala's putative major output center [Pitkanen et al., 1997;Solano-Castiella et al., 2010]. Integration of information originating from various intraamygdalar circuits in the CM is likely to mediate behavioral and autonomic responses [Pessoa, 2010] as well as to facilitate attention to salient environmental cues [Barbour et al., 2010;Kapp et al., 1994]. This accords well with the observation of specific coactivation of the CM with the posterior mid-cingulate cortex (pMCC), primary motor cortex, supplementary motor area, basal ganglia, primary somatosensory cortex, insula, and thalamus. ...
Although the amygdala complex is a brain area critical for human behavior, knowledge of its subspecialization is primarily derived from experiments in animals. We here employed methods for large-scale data mining to perform a connectivity-derived parcellation of the human amygdala based on whole-brain coactivation patterns computed for each seed voxel. Voxels within the histologically defined human amygdala were clustered into distinct groups based on their brain-wide coactivation maps. Using this approach, connectivity-based parcellation divided the amygdala into three distinct clusters that are highly consistent with earlier microstructural distinctions. Meta-analytic connectivity modelling then revealed the derived clusters' brain-wide connectivity patterns, while meta-data profiling allowed their functional characterization. These analyses revealed that the amygdala's laterobasal nuclei group was associated with coordinating high-level sensory input, whereas its centromedial nuclei group was linked to mediating attentional, vegetative, and motor responses. The often-neglected superficial nuclei group emerged as particularly sensitive to olfactory and probably social information processing. The results of this model-free approach support the concordance of structural, connectional, and functional organization in the human amygdala and point to the importance of acknowledging the heterogeneity of this region in neuroimaging research. Hum Brain Mapp, 2012. © 2012 Wiley Periodicals, Inc.
... When several stimuli compete for attention, the amygdala might contribute to the prioritization of social stimuli by pairing the encoding of their location with their motivational significance (Maunsell, 2004). Alternatively, the amygdala might contribute to attentional reorienting by means of increasing vigilance promoting arousal (Davis & Whalen, 2001) which is the more traditional understanding of the amygdala's working (Belova et al., 2007;Kapp et al., 1994). As the activity of rewardpredictive neurons differed depending on where stimuli were presented (Peck et al., 2013), these results yet speak in favor of the amygdala's involvement in the allocation of attention rather than a general increase in vigilance which should in theory yield equal activation independent of stimulus location. ...
Humans in our environment are of special importance to us. Even if our minds are fixated on tasks unrelated to their presence, our attention will likely be drawn towards other people’s appearances and their actions. While we might remain unaware of this attentional bias at times, various studies have demonstrated the preferred visual scanning of other humans by recording eye movements in laboratory settings. The present thesis aims to investigate the circumstances under and the mechanisms by which this so-called social attention operates. The first study demonstrates that social features in complex naturalistic scenes are prioritized in an automatic fashion. After 200 milliseconds of stimulus presentation, which is too brief for top-down processing to intervene, participants targeted image areas depicting humans significantly more often than would be expected from a chance distribution of saccades. Additionally, saccades towards these areas occurred earlier in time than saccades towards non-social image regions. In the second study, we show that human features receive most fixations even when bottom-up information is restricted; that is, even when only the fixated region was visible and the remaining parts of the image masked, participants still fixated on social image regions longer than on regions without social cues. The third study compares the influence of real and artificial faces on gaze patterns during the observation of dynamic naturalistic videos. Here we find that artificial faces, belonging to humanlike statues or machines, significantly predicted gaze allocation but to a lesser extent than real faces. In the fourth study, we employed functional magnetic resonance imaging to investigate the neural correlates of reflexive social attention. Analyses of the evoked blood-oxygenation level dependent responses pointed to an involvement of striate and extrastriate visual cortices in the encoding of social feature space. Collectively, these studies help to elucidate under which circumstances social features are prioritized in a laboratory setting and how this prioritization might be achieved on a neuronal level. The final experimental chapter addresses the question whether these laboratory findings can be generalized to the real world. In this study, participants were introduced to a waiting room scenario in which they interacted with a confederate. Eye movement analyses revealed that gaze behavior heavily depended on the social context and were influenced by whether an interaction is currently desired. We further did not find any evidence for altered gaze behavior in socially anxious participants. Alleged gaze avoidance or hypervigilance in social anxiety might thus represent a laboratory phenomenon that occurs only under very specific real-life conditions. Altogether the experiments described in the present thesis thus refine our understanding of social attention and simultaneously challenge the inferences we can draw from laboratory research.
... The CeA, however, may have many more complex functions that transcend associative, 37,66 response selection, 60 attentional, 67 and arousal 68,69 processes. There is little, however, to suggest that any of these processes occur within the NAcc shell, with which the CeA has neuroanatomical and connectional affinity. ...
Only recently have the functional implications of the organization of the ventral striatum, amygdala, and related limbic-cortical structures, and their neuroanatomical interactions begun to be clarified. Processes of activation and reward have long been associated with the NAcc and its dopamine innervation, but the precise relationships between these constructs have remained elusive. We have sought to enrich our understanding of the special role of the ventral striatum in coordinating the contribution of different functional subsystems to confer flexibility, as well as coherence and vigor, to goal-directed behavior, through different forms of associative learning. Such appetitive behavior comprises many subcomponents, some of which we have isolated in these experiments to reveal that, not surprisingly, the mechanisms by which an animal sequences responding to reach a goal are complex. The data reveal how the different components, pavlovian approach (or sign-tracking), conditioned reinforcement (whereby pavlovian stimuli control goal-directed action), and also more general response-invigorating processes (often called “activation,”“stress,” or “drive”) may be integrated within the ventral striatum through convergent interactions of the amygdala, other limbic cortical structures, and the mesolimbic dopamine system to produce coherent behavior. The position is probably not far different when considering aversively motivated behavior. Although it may be necessary to employ simplified, even abstract, paradigms for isolating these mechanisms, their concerted action can readily be appreciated in an adaptive, functional setting, such as the responding by rats for intravenous cocaine under a second-order schedule of reinforcement. Here, the interactions of primary reinforcement, psychomotor activation, pavlovian conditioning, and the control that drug cues exert over the integrated drug-seeking response can be seen to operate both serially and concurrently. The power of our analytic techniques for understanding complex motivated behavior has been evident for some time. However, the crucial point is that we are now able to map these components with increasing certainty onto discrete amygdaloid, and other limbic cortical-ventral striatal subsystems. The neural dissection of these mechanisms also serves an important theoretical purpose in helping to validate the various hypothetical constructs and further developing theory. Major challenges remain, not the least of which is an understanding of the operation of the ventral striatum together with its dopaminergic innervation and its interactions with the basolateral amygdala, hippocampal formation, and prefrontal cortex at a more mechanistic, neuronal level.
... Growing evidence also indicates that the amygdala is an important modulator in both NREM and REM sleep, although it is not the primary brain region involved in sleepewake regulation. Electrical stimulation of CeA suppresses delta wave activity in the frontal cortex and increases arousal (Kapp et al., 1994), and inactivation of CeA with tetrodotoxin decreases REM sleep and increases slow wave sleep (Tang et al., 2005). CBD is the first compound isolated from the cannabis plant and exhibits a broad pharmacological profile, including anti-convulsion, sedation, antianxiety, hypnotic effect, anti-psychosis and anti-inflammation (Mechoulam et al., 2002). ...
... This led to proposals that such pathways might regulate perceptual analysis of emotional stimuli, particularly when these are threat-related. As indirect support for this idea, electrical stimulation of amygdala nuclei in the rat can produce desynchronization of EEG activity in remote cortical areas, including visual cortex (Kapp et al. 1994; Dringenberg et al. 2001). Furthermore, in rats, lesions of the amygdala after auditory fear-conditioning can suppress a late amplification exhibited by auditory cortex neurons for fear-conditioned tones relative to neutral tones, while leaving the initial auditory response unchanged (Armony et al. 1998). ...
Visual processing is not determined solely by retinal inputs. Attentional modulation can arise when the internal attentional state (current task) of the observer alters visual processing of the same stimuli. This can influence visual cortex, boosting neural responses to an attended stimulus. Emotional modulation can also arise, when affective properties (emotional significance) of stimuli, rather than their strictly visual properties, influence processing. This too can boost responses in visual cortex, as for fear-associated stimuli. Both attentional and emotional modulation of visual processing may reflect distant influences upon visual cortex, exerted by brain structures outside the visual system per se. Hence, these modulations may provide windows onto causal interactions between distant but interconnected brain regions. We review recent evidence, noting both similarities and differences between attentional and emotional modulation. Both can affect visual cortex, but can reflect influences from different regions, such as fronto-parietal circuits versus the amygdala. Recent work on this has developed new approaches for studying causal influences between human brain regions that may be useful in other cognitive domains. The new methods include application of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) measures in brain-damaged patients to study distant functional impacts of their focal lesions, and use of transcranial magnetic stimulation concurrently with fMRI or EEG in the normal brain. Cognitive neuroscience is now moving beyond considering the putative functions of particular brain regions, as if each operated in isolation, to consider, instead, how distinct brain regions (such as visual cortex, parietal or frontal regions, or amygdala) may mutually influence each other in a causal manner.
... A number of hypotheses have been proposed suggesting that the amygdala may modulate mnemonic and attentional processing in cortical areas (Kapp et al., 1992;Rolls, 1992;Gallagher and Holland, 1994;McGaugh et al., 1995;Packard et al., 1995;Weinberger, 1995;Cahill and McGaugh, 1996;Armony et al., 1997b). For example, stimulation of the central nucleus produces neocortical arousal, which is mediated by cholinergic projections from the basal forebrain in rabbit (Kapp et al., 1994), and stimulation of the nucleus basalis produces facilitation of neuronal responses to tones in auditory cortex in awake rats (Edeline et al., 1994). Furthermore, pairing of a tone with iontophoretic application of ACh induces frequency-specific changes in auditory cortex neurons, similar to those observed during fear conditioning (Metherate and Weinberger, 1990). ...
In auditory fear conditioning, pairing of a neutral acoustic conditioned stimulus (CS) with an aversive unconditioned stimulus (US) results in an enhancement of neural responses to the CS in the amygdala and auditory cortex. It is not clear, however, whether cortical plasticity governs neural changes in the amygdala or vice versa, or whether learning in these two structures is determined by independent processes. We examined this issue by recording single-cell activity in the auditory cortex (areas Te1, Te1v, and Te3) of freely behaving, amygdalectomized rats using a movable bundle of microwires. Amygdala damage did not affect short-latency (0-50 msec) tone responses, nor did it interfere with conditioning-induced increases of these onset responses. In contrast, lesions of the amygdala interfered with the development of late (500-1500 msec) conditioned tone responses that were not present before conditioning. Furthermore, whereas onset conditioned responses in the control group remained elevated after 30 extinction trials (presentation of CS alone), onset responses in lesioned animals returned to their preconditioning firing level after approximately 10 extinction trials. These results suggest that the amygdala enables the development of long-latency (US anticipatory) responses and prevents the extinction of short-latency onset responses to threatening stimuli. The findings further suggest that auditory cortex cells may participate differently in explicit and implicit memory networks.
... Modern studies have picked up on some of these early themes. For instance, Kapp and colleagues reported that, in rabbits, electrical stimulation of the central amygdala suppresses low-frequency activity, namely it produces desynchronization (Kapp, Supple, & Whalen, 1994); see also (Stock, Rupprecht, Stumpf, & Schlor, 1981). Because of the well established role of the cholinergic system in cortical activation and arousal (Sarter & Bruno, 2000), Kapp and colleagues investigated the potential effects of a cholinergic antagonist during amygdala stimulation. ...
The amygdala is a fascinating, complex structure that lies at the center of much of our current thinking about emotion. Here, I will review data that suggest that the amygdala is involved in several processes linked to determining what a stimulus is and what the organism should therefore do - the two questions that are part of the title. This piece will focus on three main aspects of amygdala function, namely attention, value representation, and decision making, by reviewing both non-human and human data. Two mechanisms of affective attention will be described. The first involves projections from the central nucleus of the amygdala to the basal forebrain, which has extensive and diffuse projections throughout the cortical mantle. The second involves projections from the basal amygdala to multiple levels across the visual cortex. I will also describe how the basolateral amygdala is important for the representation of value and in decision making. Overall, it will be argued that the amygdala plays a key role in solving the following problem: How can a limited-capacity information processing system that receives a constant stream of diverse inputs be designed to selectively process those inputs that are most significant to the objectives of the system? "What is it?" and "What's to be done?" processes can then be viewed as important building blocks in the construction of emotion, a process that is intertwined with cognition. Furthermore, answering the two questions directs how resources should be mobilized as the organism seeks out additional information from the environment.
... Bradley (2009) pointed out that the HR deceleration in humans appears equivalent to "fear bradycardia" of most mammals, i.e., the rapid slowing of heart rate with accompanied behavioral "freezing" when the animal is confronted with a threatening stimulus. The role of the amygdala in the threat-related orienting response was highlighted by Kapp, Supple, and Whalen (1994) who showed that direct stimulation of the amygdala results in HR deceleration and increased cortical arousal in animals. Thus, the HR deceleration response to threat-related cues may be part of a defenserelated orienting reflex that acts to facilitate perceptual processing and extraction of information about potentially significant stimuli (Bradley, 2009). ...
Orienting of attention to emotionally negative stimuli is accompanied by rapid heart rate (HR) deceleration, reflecting enhanced attentional and sensory processing. We studied whether similar emotional modulation of cardiac responding is observed in infants. HR and eye movements were recorded from 7-month-old infants while they observed a fearful or happy face that was flanked after 700 ms by a peripheral distractor for 2000 ms. An attentional bias for fearful faces was indicated by less frequent and longer latency saccades toward the distractors during fearful than happy trials. HR deceleration was significantly larger during fearful than happy trials on which infants did not make a distractor-directed saccade. For trials with a distractor-directed saccade, no difference between fearful and happy faces emerged. Thus, the bias to attend preferentially to fearful faces is accompanied by a concomitant increase in the cardiac orienting response.
... In the present study, the pre-stimulus GRC of amygdala upon hippocampus may be related to vigilance as the subject attends the next painful stimulus in a random series of such stimuli. Involvement of the amygdala in attention is supported by studies demonstrating that anticipation leads to increased neuronal activity in the primate amygdala (Belova et al., 2008), and stimulation of the central nucleus leads to low voltage fast EEG activity (Kapp et al., 1994), as well as orienting responses (Applegate et al., 1983; Davis and Whalen, 2001). ...
The pathways by which painful stimuli are signaled within the human medial temporal lobe are unknown. Rodent studies have shown that nociceptive inputs are transmitted from the brainstem or thalamus through one of two pathways to the central nucleus of the amygdala. The indirect pathway projects from the basal and lateral nuclei of the amygdala to the central nucleus, while the direct pathway projects directly to the central nucleus. We now test the hypothesis that the human ventral amygdala (putative basal and lateral nuclei) exerts a causal influence upon the dorsal amygdala (putative central nucleus), during the application of a painful laser stimulus. Local field potentials (LFPs) were recorded from depth electrode contacts implanted in the medial temporal lobe for the treatment of epilepsy, and causal influences were analyzed by Granger causality (GRC). This analysis indicates that the dorsal amygdala exerts a pre-stimulus causal influence upon the hippocampus, consistent with an attention-related response to the painful laser. Within the amygdala, the analysis indicates that the ventral contacts exert a causal influence upon dorsal contacts, consistent with the human (putative) indirect pathway. Potentials evoked by the laser (LEPs) were not recorded in the ventral nuclei, but were recorded at dorsal amygdala contacts which were not preferentially those receiving causal influences from the ventral contacts. Therefore, it seems likely that the putative indirect pathway is associated with causal influences from the ventral to the dorsal amygdala, and is distinct from the human (putative) indirect pathway which mediates LEPs in the dorsal amygdala.
... In rabbits, electrical stimulation of the CE induces responses that are normally induced by threatening stimuli, such as bradycardia, increases in respiration, pupil dilation and freezing (Applegate, Kapp, Underwood, & McNall, 1983). Furthermore, electrical CE stimulation arouses the cortex by suppressing the occurrence of slow delta waves in the EEG and inducing fast-frequency low-amplitude waves (B. S. Kapp, Supple, & Whalen, 1994). Since this EEG pattern is thought to be established by increased cholinergic neurotransmission, this suggests that projections from CE to the magnocellular basal nucleus are involved in this effect . ...
... The mechanistic basis of the slow return to baseline activities after the arousal is unclear although it is similar to the slow return of low-frequency, high-amplitude cortical activity after electrical stimulation of the brainstem or of the amygdala which transiently evokes high-frequency, low-amplitude activity (Kapp et al., 1994; Whalen et al., 1994; Curto et al., 2009). We have also reported a slow return of C3A2 mutual information to its baseline state following arousals, as well as a slow return of coupling between C3A2 and C4A1 EEG signals (Ramanand et al., 2010). ...
Arousals are often considered to be events which have an abrupt onset and offset, indicating abrupt changes in the state of the cortex. We hypothesized that cortical state, as reflected in electroencephalograph (EEG) signals, exhibits progressive systematic changes before and after a spontaneous, isolated arousal and that the time courses of the spectral components of the EEG before and after an arousal would differ between healthy middle-aged and elderly subjects. We analyzed the power spectrum and Sample Entropy of the C3A2 EEG before and after isolated arousals from 20 middle-aged (47.2±2.0 years) and 20 elderly (78.4±3.8 years) women using polysomnograms from the Sleep Heart Health Study database. In middle-aged women, all EEG spectral band powers <16 Hz exhibited a significant increase relative to baseline at some time in the 21 s before an arousal, but only low- (0.2-2.0 Hz) and high-frequency (2.0-4.0 Hz) delta increased in elderly and only during the last 7 s pre-arousal. Post-arousal, all frequency bands below 12 Hz transiently fell below pre-arousal baseline in both age groups. Consistent with these findings, Sample Entropy decreased steadily before an arousal, increased markedly during the arousal, and remained above pre-arousal baseline levels for ∼30 s after the arousal. In middle-aged, but not in elderly, women the presence of early pre-arousal low delta power was associated with shorter arousals. We propose that this attenuation of the effect of the arousing stimulus may be related to the slow (<1 Hz) cortical state oscillation, and that prolonged alterations of cortical state due to arousals may contribute to the poor correlation between indices of arousals and indices of sleepiness or impaired cognitive function.
... The role of amygdala on arousal and wakefulness has been emphasized. Electrical stimulation of CeA suppresses delta wave activity in the frontal cortex and increases neocortical arousal [42]. Although our result demonstrated that administration of naloxone into CeA did not alter sleep activities in naïve rats, opioids could inhibit both excitability of pyramidal cells [43] and GABAergic interneurons [44] in the CeA. ...
Clinical and experimental evidence demonstrates that sleep and epilepsy reciprocally affect each other. Previous studies indicated that epilepsy alters sleep homeostasis; in contrast, sleep disturbance deteriorates epilepsy. If a therapy possesses both epilepsy suppression and sleep improvement, it would be the priority choice for seizure control. Effects of acupuncture of Feng-Chi (GB20) acupoints on epilepsy suppression and insomnia treatment have been documented in the ancient Chinese literature, Lingshu Jing (Classic of the Miraculous Pivot). Therefore, this study was designed to investigate the effect of electroacupuncture (EA) stimulation of bilateral Feng-Chi acupoints on sleep disruptions in rats with focal epilepsy.
Our result indicates that administration of pilocarpine into the left central nucleus of amygdala (CeA) induced focal epilepsy and decreased both rapid eye movement (REM) sleep and non-REM (NREM) sleep. High-frequency (100 Hz) EA stimulation of bilateral Feng-Chi acupoints, in which a 30-min EA stimulation was performed before the dark period of the light:dark cycle in three consecutive days, further deteriorated pilocarpine-induced sleep disruptions. The EA-induced exacerbation of sleep disruption was blocked by microinjection of naloxone, mu- (naloxonazine), kappa- (nor-binaltorphimine) or delta-receptor antagonists (natrindole) into the CeA, suggesting the involvement of amygdaloid opioid receptors.
The present study suggests that high-frequency (100 Hz) EA stimulation of bilateral Feng-Chi acupoints exhibits no benefit in improving pilocarpine-induced sleep disruptions; in contrast, EA further deteriorated sleep disturbances. Opioid receptors in the CeA mediated EA-induced exacerbation of sleep disruptions in epileptic rats.
... and dangerous situations (Endler et al., 1992). Studies investigating the neurobiological basis of anxiety have implicated the amygdala in various negative affective responses, including the fear and vigilance that are characteristic of anxiety (Kapp et al., 1994;Oler et al., 2009;Pessoa and Adolphs, 2010;Whalen, 1998). An increasing number of studies have linked anxiety to complex functional and structural neural circuitry that is centered on the amygdala (Kim et al., 2011a). ...
Objective:
A current neuroanatomical model of anxiety posits that greater structural connectivity between the amygdala and ventral prefrontal cortex (vPFC) facilitates regulatory control over the amygdala and helps reduce anxiety. However, some neuroimaging studies have reported contradictory findings, demonstrating a positive rather than negative association between trait anxiety and amygdala-vPFC white matter integrity. To help reconcile these findings, we tested the regulatory hypothesis of anxiety circuitry using aging as a model of white matter decline in the amygdala-vPFC pathway.
Methods:
We used probabilistic tractography to trace connections between the amygdala and vPFC in 21 younger, 18 middle-aged, and 15 healthy older adults. The resulting tract estimates were used to extract 3 indices of white-matter integrity: fractional anisotropy (FA), radial diffusivity (RD), and axial diffusivity (AD). The relationship between these amygdala-vPFC structural connectivity measures and age and State-Trait Anxiety Inventory (STAI) scores were assessed.
Results:
The tractography results revealed age-related decline in the FA (p = .005) and radial diffusivity (p = .002) of the amygdala-vPFC pathway. Contrary to the regulatory hypothesis, we found a positive rather than negative association between trait anxiety and right amygdala-vPFC FA (p = .01).
Conclusion:
These findings argue against the notion that greater amygdala-vPFC structural integrity facilitates better anxiety outcomes in healthy adults. Instead, our results suggest that white matter degeneration in this network relates to lower anxiety in older adults.
... Systemic administration of centrally acting muscarinic receptor antagonists could block the cholinergically mediated neocortical arousal by unilateral electrical stimulation of the amygdaloid central nucleus (ACe). These results suggested the involvement of the BF in amygdala-induced arousal (McDonald 1991;Kapp et al. 1994;Dringenberg and Vanderwolf 1996). However, microscopic studies showed that paradoxical results, the existence of glutamatergic inputs and the inhibitory GABAergic inputs from the amygdala to BF (Zaborszky et al. 1984;Pare and Smith 1994), are in line with an early study that there were antergic glutamatergic and GABAergic systems in the basolateral amygdala that one desynchronizes while another one synchronizes the neocortex activity (Kreindler and Steriade 1964). ...
In mammals, parental care is essential for the survival of the young; therefore, it is vitally important to the propagation of the species. These behaviors, differing between the two sexes, are innate, stereotyped, and are also modified by an individual’s reproductive experience. These characteristics suggest that neural mechanisms underlying parental behaviors are genetically hardwired, evolutionarily conserved as well as sexually differentiated and malleable to experiential changes. Classical lesion studies on neural control of parental behaviors, mostly done in rats, date back to the 1950s. Recent developments of new methods and tools in neuroscience, which allow precise targeting and activation/inhibition of specific populations of neurons and their projections to different brain structures, have afforded fresh opportunities to dissect and delineate the detailed neural circuit mechanisms that govern distinct components of parental behaviors in the genetically tractably organism, the laboratory mouse (Mus musculus). In this review, we summarize recent discoveries using modern neurobiological tools within the context of traditional lesion studies. In addition, we discuss interesting cross talk between neural circuits that govern parent care with those that regulate other innate behaviors such as feeding and mating.
... Systemic administration of centrally acting muscarinic receptor antagonists could block the cholinergically mediated neocortical arousal by unilateral electrical stimulation of the amygdaloid central nucleus (ACe). These results suggested the involvement of the BF in amygdala-induced arousal (McDonald 1991;Kapp et al. 1994;Dringenberg and Vanderwolf 1996). However, microscopic studies showed that paradoxical results, the existence of glutamatergic inputs and the inhibitory GABAergic inputs from the amygdala to BF (Zaborszky et al. 1984;Pare and Smith 1994), are in line with an early study that there were antergic glutamatergic and GABAergic systems in the basolateral amygdala that one desynchronizes while another one synchronizes the neocortex activity (Kreindler and Steriade 1964). ...
Fear is defined as a fundamental emotion promptly arising in the context of threat and when danger is perceived. Fear can be innate or learned. Examples of innate fear include fears that are triggered by predators, pain, heights, rapidly approaching objects, and ancestral threats such as snakes and spiders. Animals and humans detect and respond more rapidly to threatening stimuli than to nonthreatening stimuli in the natural world. The threatening stimuli for most animals are predators, and most predators are themselves prey to other animals. Predatory avoidance is of crucial importance for survival of animals. Although humans are rarely affected by predators, we are constantly challenged by social threats such as a fearful or angry facial expression. This chapter will summarize the current knowledge on brain circuits processing innate fear responses to visual stimuli derived from studies conducted in mice and humans.
... The laterobasal nuclei group is believed to send its highly preprocessed information mostly towards the centromedial group, the amygdala's putative major output center [Pitkanen et al., 1997;Solano-Castiella et al., 2010]. Integration of information originating from various intraamygdalar circuits in the CM is likely to mediate behavioral and autonomic responses [Pessoa, 2010] as well as to facilitate attention to salient environmental cues [Barbour et al., 2010;Kapp et al., 1994]. This accords well with the observation of specific coactivation of the CM with the posterior mid-cingulate cortex (pMCC), primary motor cortex, supplementary motor area, basal ganglia, primary somatosensory cortex, insula, and thalamus. ...
... The significant correlation between resting activity of the CM nuclei and signal fluctuation from areas attributed to the salience network (SN), e.g., anterior insula, ACC and middle cingulate cortex (MCC) 50 , is consistent with the central nucleus involvement in facilitating attention to salient stimuli 51 . In addition, the CM was the only amygdala subdivision in which the rsFC pattern predicted activation in response to fear and angry faces, thus indicating its association with adverse feelings. ...
Similarities on the cellular and neurochemical composition of the amygdaloid subnuclei suggests their clustering into subunits that exhibit unique functional organization. The topological principle of community structure has been used to identify functional subnetworks in neuroimaging data that reflect the brain effective organization. Here we used modularity to investigate the organization of the amygdala using resting state functional magnetic resonance imaging (rsfMRI) data. Our goal was to determine whether such topological organization would reliably reflect the known neurobiology of individual amygdaloid nuclei, allowing for human imaging studies to accurately reflect the underlying neurobiology. Modularity analysis identified amygdaloid elements consistent with the main anatomical subdivisions of the amygdala that embody distinct functional and structural properties. Additionally, functional connectivity pathways of these subunits and their correlation with task-induced amygdala activation revealed distinct functional profiles consistent with the neurobiology of the amygdala nuclei. These modularity findings corroborate the structure-function relationship between amygdala anatomical substructures, supporting the use of network analysis techniques to generate biologically meaningful partitions of brain structures.
... On the other hand, the source of threat related to fear is more ambiguous thus requiring additional contextual information on part of the addressed agent (Pichon, de Gelder, & Grèzes, 2009). With increasing ambiguity, there is greater activation of neural circuitry associated with increasing attention and vigilance towards environmental stimuli via the modulation of response thresholds of sensory cortical neurons (Kapp, Supple, & Whalen, 1994;Weinberger et al., 1990;Whalen, 1998), so as to increase the likelihood of acquiring additional information (about the source of threat). Accordingly, there is a body of work indicating that anger and fear differentially perturb emotion processing circuitry (Adolphs, Tranel, Damasio, & Damasio, 1994Broks et al., 1998;Calder et al., 1996;Whalen et al., 2001). ...
Although the Behavioral Inhibition System (BIS) is associated with threat-sensitivity, little is known about its neurofunctional correlates during cognitive control over task-irrelevant threat distractors. Thirty non-clinical participants, who ranged in BIS sensitivity, completed an attentional control paradigm during fMRI. The paradigm varied in cognitive demand with low perceptual load comprising identical target letters and high perceptual load comprising a target letter in a mixed letter string; each superimposed on threatening and neutral face distractors. Whole-brain results indicated that individuals with higher, relative to lower BIS sensitivity, exhibited enhanced dorsolateral prefrontal cortex activation to angry (vs. neutral) and enhanced dorsal anterior cingulate cortex activation to fearful (vs. neutral) face distractors under low load whereas no differences in activation were observed under high load. These findings are consistent with literature indicating that the BIS is involved in conflict processing, including between cognitive and emotional or motivational goals.
... Neurons in the central nucleus of the amygdala (CeA) project to the NBM (Jolkkonen, Miettinen, Pikkarainen, and Pitkanen, 2002;McDonald, 1991;Petrovich and Swanson, 1997;Price and Amaral, 1981), and given the role of the CeA in conditioned fear memory (Goosens and Maren, 2001;Wilensky, Schafe, Kristensen, and LeDoux, 2006), CeA input to NBM cholinergic neurons could stimulate ACh release in the PFC and induce plasticity critical for fear memory in the conditioned suppression paradigm (i.e. CeANBMPFC) (Kapp, Supple, and Whalen, 1994;Weinberger, 1998). CeA neurons predominantly terminate on GABAergic neurons in the NBM (Jolkkonen et al., 2002), which suggests for the CeANBMPFC circuit to be valid, CeA input to the NBM would have to act via GABAergic NBM neurons (Jolkkonen et al., 2002). ...
Cholinergic input to the neocortex, dorsal hippocampus (dHipp), and basolateral amygdala (BLA) is critical for neural function and synaptic plasticity in these brain regions. Synaptic plasticity in the neocortex, dHipp, ventral Hipp (vHipp), and BLA has also been implicated in fear and extinction memory. This finding raises the possibility that basal forebrain (BF) cholinergic neurons, the predominant source of acetylcholine in these brain regions, have an important role in mediating fear and extinction memory. While empirical studies support this hypothesis, there are interesting inconsistencies among these studies that raise questions about how best to define the role of BF cholinergic neurons in fear and extinction memory. Nucleus basalis magnocellularis (NBM) cholinergic neurons that project to the BLA are critical for fear memory and contextual fear extinction memory. NBM cholinergic neurons that project to the neocortex are critical for cued and contextual fear conditioned suppression, but are not critical for fear memory in other behavioral paradigms and in the inhibitory avoidance paradigm may even inhibit contextual fear memory formation. Medial septum and diagonal band of Broca cholinergic neurons are critical for contextual fear memory and acquisition of cued fear extinction. Thus, even though the results of previous studies suggest BF cholinergic neurons modulate fear and extinction memory, inconsistent findings among these studies necessitates more research to better define the neural circuits and molecular processes through which BF cholinergic neurons modulate fear and extinction memory. Furthermore, studies determining if BF cholinergic neurons can be manipulated in such a manner so as to treat excessive fear in anxiety disorders are needed.
The neural mechanisms of sleep, a fundamental biological behavior from invertebrates to humans, have been a long-standing mystery and present an enormous challenge. Gradually, perspectives on the neurobiology of sleep have been more various with the technical innovations over the recent decades, and studies have now identified many specific neural circuits that selectively regulate the initiation and maintenance of wake, rapid eye movement (REM) sleep, and non-REM (NREM) sleep. The cholinergic system in basal forebrain (BF) that fire maximally during waking and REM sleep is one of the key neuromodulation systems related to waking and REM sleep. Here we outline the recent progress of the BF cholinergic system in sleep–wake cycle. The intricate local connectivity and multiple projections to other cortical and subcortical regions of the BF cholinergic system elaborately presented here form a conceptual framework for understanding the coordinating effects with the dissecting regions. This framework also provides evidences regarding the relationships between the general anesthesia and wakefulness/sleep cycle focusing on the neural circuitry of unconsciousness induced by anesthetic drugs.
This article explores the role of music, along with other modes of expression, in the production of emotion in three distinct religious rituals in Bogotá. The research sought to prove the theoretical concept of “worlds of sense,” within which greater correlation between the contents of different signifying languages not only produces greater emotional intensity but also delineates what behaviors are possible. To accomplish this, interviews and questionnaires were completed, the expressive material of each ritual was analyzed, and the emotional response of nine subjects was measured through physical behavior and electro-encephalographic measurements. The analysis allowed us to conclude that the ritual with less predictability and greater concordance between music and other significant elements is also the ritual in which emotions are expressed with greater intensity and the mandates of the church/mosque are followed more rigorously, while rituals with predictable structures and greater contradiction between the musical and other key elements show less emotional intensity and a lower level of obedience. However, it is impossible to establish a direct causal relationship between the expressive material and the emotional response. Towards the end of the article, other lines of inquiry are proposed to examine the potential of music to influence behavior in the context of multimodal reinforcement experiences.
Anesthesia, slow-wave sleep, syncope, concussion and reversible coma are behavioral states characterized by loss of consciousness, slow-wave cortical electroencephalogram, and motor and sensory suppression. We identified a focal area in the rat brainstem, the mesopontine tegmental anesthesia area (MPTA), at which microinjection of pentobarbital and other GABA(A) receptor (GABA(A)-R) agonists reversibly induced an anesthesia-like state. This effect was attenuated by local pre-treatment with the GABA(A)-R antagonist bicuculline. Using neuroanatomical tracing we identified four pathways ascending from the MPTA that are positioned to mediate electroencephalographic synchronization and loss of consciousness: (i) projections to the intralaminar thalamic nuclei that, in turn, project to the cortex; (ii) projections to several pontomesencephalic, diencephalic and basal forebrain nuclei that project cortically and are considered parts of an ascending "arousal system"; (iii) a projection to other parts of the subcortical forebrain, including the septal area, hypothalamus, zona incerta and striato-pallidal system, that may indirectly affect cortical arousal and hippocampal theta rhythm; and (iv) modest projections directly to the frontal cortex. Several of these areas have prominent reciprocal projections back to the MPTA, notably the zona incerta, lateral hypothalamus and frontal cortex. We hypothesize that barbiturate anesthetics and related agents microinjected into the MPTA enhance the inhibitory response of local GABA(A)-R-bearing neurons to endogenous GABA released at baseline during wakefulness. This modulates activity in one or more of the identified ascending neural pathways, ultimately leading to loss of consciousness.
Contextual fear is followed by significant reductions in rapid eye movement sleep (REM) that are regulated by the central nucleus of the amygdala (CNA). Corticotropin-releasing factor (CRF) plays a major role in regulating the stress response as well as arousal, and CRF in CNA is implicated in stress-related behavior. To test the hypothesis that CRF regulation of CNA is involved in fear-induced alterations in REM, we determined the effects of microinjections into CNA of the CRF1 antagonist, antalarmin (ANT) on fear-induced reductions in REM. We also evaluated c-Fos activation in the hypothalamic paraventricular nucleus (PVN), locus coeruleus (LC), and dorsal raphe nucleus (DRN) to determine whether activation of these regions was consistent with their roles in regulating stress and in the control of REM.
On separate days, rats were subjected to baseline and 2 shock training sessions (S1 and S2). Five days later, the rats received bilateral microinjections of ANT (4.8 mM) or vehicle (VEH) prior to exposure to the fearful context. Sleep was recorded for 20 h in each condition. Freezing was assessed during S1, S2, and context. Separate groups of rats received identical training and microinjections or handling control (HC) only, but were sacrificed 2 h after context exposure to assess c-Fos expression.
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Compared to baseline, S1 and S2 significantly reduced REM. Exposure to the fearful context reduced REM in VEH treated rats, whereas REM in ANT treated rats did not differ from baseline. ANT did not significantly alter freezing. Fear-induced c-Fos expression was decreased in PVN and LC after ANT compared to VEH.
The results demonstrate that CRF receptors in CNA are involved in fear-induced reductions in REM and neural activation (as indicated by c-Fos) in stress and REM regulatory regions, but not in fear-induced freezing.
In altricial species, like the human, the caregiver, very often the mother, is one of the most potent stimuli during development. The distinction between mothers and other adults is learned early in life and results in numerous behaviors in the child, most notably mother-approach and stranger wariness. The current study examined the influence of the maternal stimulus on amygdala activity and related circuitry in 25 developing children (n = 13) and adolescents (n = 12), and how this circuitry was associated with attachment-related behaviors. Results indicated that maternal stimuli were especially effective in recruiting activity in the left dorsal amygdala, and activity in this amygdala region showed increased functional connectivity with evaluative and motor regions during viewing of maternal stimuli. Increases in this left dorsal amygdala activity and related amygdala-cortical functional connectivity were associated with increased mother-approach behaviors as measured by in-scanner behavioral responding and out-of-scanner child-report. Moreover, age-related changes in amygdala activity to strangers statistically mediated the developmentally typical decline in stranger wariness seen across this period. These results suggest that mother-induced behaviors are enacted by maternal influence on amygdala-cortical circuitry during childhood and adolescence.
In this paper we review current definitions and measurement approaches used to assess individual differences in children’s temperament. We review the neural bases of temperamental reactivity and self-regulation and propose that these constructs provide a framework for examining individual differences and developmental change in emotion–cognition interactions across development. Studies are reviewed in which some well-documented contextual effects on the expression of temperament can be interpreted in terms of the influence of biological and non-biological factors on CNS functioning. We conclude with ideas regarding future directions for the study of individual differences and developmental change in cognition–emotion interactions as they are shaped throughout development.
Pavlovian fear conditioning has emerged as a leading behavioral paradigm for studying the neurobiological basis of learning and memory. Although considerable progress has been made in understanding the neural substrates of fear conditioning at the systems level, until recently little has been learned about the underlying cellular and molecular mechanisms. The success of systems-level work aimed at defining the neuroanatomical pathways underlying fear conditioning, combined with the knowledge accumulated by studies of long-term potentiation (LTP), has recently given way to new insights into the cellular and molecular mechanisms that underlie acquisition and consolidation of fear memories. Collectively, these findings suggest that fear memory consolidation in the amygdala shares essential biochemical features with LTP, and hold promise for understanding the relationship between memory consolidation and synaptic plasticity in the mammalian brain.
This article is a review of the results of a series of experiments designed to identify brain systems involved in appetitive
conditioning of rats. It discusses some of their implications for behavioral theories of learning, especially those that concern
changes in processing of conditioned stimuli (CSs). Evidence is presented which suggests that separable brain circuits are
involved in (1) the production of CS-dependent conditioned orienting responses, (2) the enhancement of CS associability produced
when expectancies about upcoming events are violated, (3) the reduction of CS associability produced when stimuli are consistent
predictors of other events or are presented without consequence, and (4) the abilities of CSs to serve as reinforcers for
second-order conditioning and to be sensitive to postconditioning changes in the value of the unconditioned stimulus (US).
Finally, none of these circuits seems critical for normal acquisition of the most common indicator of Pavlovian conditioning,
US-dependent conditioned responses (CRs). Although the independence of brain pathways does not demand independence of behavioral
function, clustering of behavioral phenomena on anatomical grounds may provide useful guides for constructing behavior theories.
In altricial species, like the human, caregiver presence is necessary for typical emotional development. Children who have been raised in institutional care early in life experience caregiver deprivation and are at significantly elevated risk for emotional difficulties. The current manuscript examines the non-human and human literatures on amygdala development following caregiver deprivation and presents an argument that in the absence of the species-expected caregiver presence, human amygdala development exhibits rapid development and perhaps premature engagement that results in some of the emotional phenotypes observed following early institutional care.
This paper will concentrate on two features of the systems described by Alheid and Heimer 1 that have influenced research in our laboratory in recent years. In the first part, we describe our findings on a representational function of the amygdaloid basolateral complex that appears to depend on its interconnections with the prefrontal cortex. In the second part, we describe progress assessing the function of magnocellular corticopetal neurons within the basal forebrain and the strong input to this system from the central amygdaloid group. These lines of behavioral research have revealed that subsystems in the basal forebrain and amygdala serve adaptive functions beyond the domains of motivation and emotion to include attention and cognition.
Cannabidiol (CBD) is one of the psycho-inactive constituents of marijuana, the Cannabis sativa. The pharma-cological property of CBD, especially the anxiolytic effect, is significant in the therapeutic purposes. The central nucleus of amygdala (CeA) plays a key role in the anxiety and its related behavioral responses (e.g. sleep-wake activity), and sero-tonin is one of the major mediators. However, the sleep-wake effect of CBD remains unclear. This study was designed to elucidate the effects of CBD on sleep-wake alteration and the involvement of serotonin in the CeA. Administrations of 5-hydroxytryptamine (5-HT), 5-HT 1A receptor partial agonist (buspirone), 5-HT 2 antagonist (ritanserin), cannabinoid CB 1 receptor agonist (ACEA), or CB 1 antagonist (AM-251) were employed to elucidate the action of CBD on CeA presynaptic CB 1 receptors, serotonergic activity and the subsequent sleep alteration. We found that microinjection of CBD into the CeA prior to the beginning of the light period dose-dependently decreased slow wave sleep (SWS) with limited effect on rapid eye movement sleep (REMS). CBD-induced SWS suppression during the light period could be mimicked by admin-istering serotonin into the CeA. Buspirone and ritanserin dose-dependently blocked CBD-induced SWS decrease. Fur-thermore, administration of AM-251 exhibits similar effect as that of CBD on sleep-wake activity, and the CBD-induced SWS decrease was partially blocked by ACEA. These observations suggest that CBD acting on the CeA neurons de-creases SWS during the light phase, which is at least partially mediated by the consequence of antagonizing presynaptic CB 1 receptors, enhancing serotonin release from the presynaptic terminals and subsequently acting on the postsynaptic 5-HT 2 receptors.
The article considers patterns of reactivity in organ systems mediated by the autonomic nervous system as they relate to central neural circuits activated by affectively arousing cues. The relationship of these data to the concept of discrete emotion and their relevance for the autonomic feedback hypothesis are discussed. Research both with animal and human participants is considered and implications drawn for new directions in emotion science. It is suggested that the proposed brain-based view has a greater potential for scientific advance than the traditional model that emphasizes specific states of mind as mediators or reflectors of visceral action.
Summary There have been a number of advances in the understanding of the neurobiology of anxiety disorders in recent years. Most of these advances have involved the study of adults, but advances have also been made in the understanding of pathologic anxiety in children. This article reviews the anatomy of normal fear and pathologic anxiety. In addition, developmental and temperamental predisposition to anxiety is also reviewed. Finally, the neurobiology of specific anxiety disorders is reviewed including data from the study of children and adults.
A stimulus predicting reinforcement can trigger emotional responses, such as arousal, and cognitive ones, such as increased attention toward the stimulus. Neuroscientists have long appreciated that the amygdala mediates spatially nonspecific emotional responses, but it remains unclear whether the amygdala links motivational and spatial representations. To test whether amygdala neurons encode spatial and motivational information, we presented reward-predictive cues in different spatial configurations to monkeys and assessed how these cues influenced spatial attention. Cue configuration and predicted reward magnitude modulated amygdala neural activity in a coordinated fashion. Moreover, fluctuations in activity were correlated with trial-to-trial variability in spatial attention. Thus, the amygdala integrates spatial and motivational information, which may influence the spatial allocation of cognitive resources. These results suggest that amygdala dysfunction may contribute to deficits in cognitive processes normally coordinated with emotional responses, such as the directing of attention toward the location of emotionally relevant stimuli.
Several studies have shown that at 7 months of age, infants display an attentional bias toward fearful facial expressions. In this study, we analyzed visual attention and heart rate data from a cross-sectional study with 5-, 7-, 9-, and 11-month-old infants (Experiment 1) and visual attention from a longitudinal study with 5- and 7-month-old infants (Experiment 2) to examine the emergence and stability of the attentional bias to fearful facial expressions. In both experiments, the attentional bias to fearful faces appeared to emerge between 5 and 7 months of age: 5-month-olds did not show a difference in disengaging attention from fearful and nonfearful faces, whereas 7- and 9-month-old infants had a lower probability of disengaging attention from fearful than nonfearful faces. Across the age groups, heart rate (HR) data (Experiment 1) showed a more pronounced and longer-lasting HR deceleration to fearful than nonfearful expressions. The results are discussed in relation to the development of the perception and experience of fear and the interaction between emotional and attentional processes.
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