The Role of the Subgenual Anterior Cingulate Cortex and Amygdala in Environmental Sensitivity to Infant Crying

This work was supported by the Swiss National Science Foundation (SNF): Grant 51A240-104890 to FHW and ES, and the Swiss National Science Foundation (SNF): Grant PA00P1_145418 to IM and the Freiwillige Akademische Gesellschaft to IM

Exploring Emotions Using Invasive Methods: Review of 60 Years of Human Intracranial Electrophysiology

Over the past 60 years, human intracranial electrophysiology (HIE) has been used to characterize seizures in patients with epilepsy. Secondary to the clinical objectives, electrodes implanted intracranially have been used to investigate mechanisms of human cognition. In addition to studies of memory and language, HIE methods have been used to investigate emotions. The aim of this review is to outline the contribution of HIE (electrocorticography, single-unit recording and electrical brain stimulation) to our understanding of the neural representations of emotions. We identified 64 papers dating back to the mid-1950s which used HIE techniques to study emotional states. Evidence from HIE studies supports the existence of widely distributed networks in the neocortex, limbic/paralimbic regions and subcortical nuclei which contribute to the representation of emotional states. In addition, evidence from HIE supports hemispheric dominance for emotional valence. Furthermore, evidence from HIE supports the existence of overlapping neural areas for emotion perception, experience and expression. Lastly, HIE provides unique insights into the temporal dynamics of neural activation during perception, experience and expression of emotional states. In conclusion, we propose that HIE techniques offer important evidence which must be incorporated into our current models of emotion representation in the human brain

Processing of nonverbal vocalisations in dementia

Nonverbal emotional vocalisations are fundamental communicative signals used to convey a diverse repertoire of social and emotional information. They transcend the boundaries of language and cultural specificity that hamper many neuropsychological tests, making them ideal candidates for understanding impaired socio-emotional signal processing in dementia. Symptoms related to changes in social behaviour and emotional responsiveness are poorly understood yet have significant impact on patients with dementia and those who care for them. In this thesis, I investigated processing of nonverbal emotional vocalisations in patients with Alzheimer’s disease and frontotemporal dementia (FTD), a disease spectrum encompassing three canonical syndromes characterised by marked socio-emotional and communication difficulties - behavioural variant FTD (bvFTD), semantic variant primary progressive aphasia (svPPA) and nonfluent/agrammatic variant primary progressive aphasia (nfvPPA). I demonstrated distinct profiles of impairment in identifying three salient vocalisations (laughter, crying and screaming) and the emotions they convey. All three FTD syndromes showed impairments, with the most marked deficits of emotion categorisation seen in the bvFTD group. Voxel-based morphometry was used to define critical brain substrates for processing vocalisations, identifying correlates of vocal sound processing with auditory perceptual regions (superior temporal sulcus and posterior insula) and emotion identification with limbic and medial frontal regions. The second half of this thesis focused on the more fine-grained distinction of laughter subtypes. I studied cognitive (labelling), affective (valence) and autonomic (pupillometric) processing of laughter subtypes representing dimensions of valence (mirthful versus hostile) and arousal (spontaneous versus posed). Again, FTD groups showed greatest impairment with profiles suggestive of primary perceptual deficits in nfvPPA, cognitive overgeneralisation in svPPA and disordered reward and hedonic valuation in bvFTD. Neuroanatomical correlates of explicit laughter identification included inferior frontal and cingulo-insular cortices whilst implicit processing (indexed as autonomic arousal) was particularly impaired in those conditions associated with insular compromise (nfvPPA and bvFTD). These findings demonstrate the potential of nonverbal emotional vocalisations as a probe of neural mechanisms underpinning socio-emotional dysfunction in neurodegenerative diseases

Neuroanthropology: Evolution and Emotional Embodiment

The Decade of the Mind is a proposal for a research initiative focused on four areas of neuroscience, including mental health, high-level cognitive function, education, and computational applications. Organizing efforts to date have primarily included cognitive scientists, computer scientists, and engineers, as well as physicians. At the same time anthropologists have started to explore the implications of neuroscience for understanding culture. Here we suggest that evolutionary neuroscience can be used to bridge knowledge obtained by social scientists with that obtained in the neurosciences for a more complete appreciation of the mind. We consider such a perspective as neuroanthropology. We use embodiment, an anthropological concept that has been substantiated by recent findings in neuroscience, to illustrate an integrative biocultural approach within neuroanthropology and suggest future possible directions for research

Time Scales of Auditory Habituation in the Amygdala and Cerebral Cortex

Habituation is a fundamental form of learning manifested by a decrement of neuronal responses to repeated sensory stimulation. In addition, habituation is also known to occur on the behavioral level, manifested by reduced emotional reactions to repeatedly presented affective stimuli. It is, however, not clear which brain areas show a decline in activity during repeated sensory stimulation on the same time scale as reduced valence and arousal experience and whether these areas can be delineated from other brain areas with habituation effects on faster or slower time scales. These questions were addressed using functional magnetic resonance imaging acquired during repeated stimulation with piano melodies. The magnitude of functional responses in the laterobasal amygdala and in related cortical areas and that of valence and arousal ratings, given after each music presentation, declined in parallel over the experiment. In contrast to this long-term habituation (43 min), short-term decreases occurring within seconds were found in the primary auditory cortex. Sustained responses that remained throughout the whole investigated time period were detected in the ventrolateral prefrontal cortex extending to the dorsal part of the anterior insular cortex. These findings identify an amygdalocortical network that forms the potential basis of affective habituation in human

Insular cortex activity and the evocation of laughter

The insular cortex is fundamentally involved in the processing of interoceptive information. It has been postulated that the integrative monitoring of the bodily responses to environmental stimuli is crucial for the recognition and experience of emotions. Because emotional arousal is known to be closely coupled to functions of the anterior insula, we suspected laughter to be associated primarily with neuronal activity in this region. An anatomically constrained re-analysis of our imaging data pertaining to ticklish laughter, to inhibited ticklish laughter, and to voluntary laughter revealed regional differences in the levels of neuronal activity in the posterior and mid-/anterior portions of the insula. Ticklish laughter was associated specifically with right ventral anterior insular activity, which was not detected under the other two conditions. Hence, apparently, only laughter that is evoked as an emotional response bears the signature of autonomic arousal in the insular cortex

Regional Brain Responses in Nulliparous Women to Emotional Infant Stimuli

Infant cries and facial expressions influence social interactions and elicit caretaking behaviors from adults. Recent neuroimaging studies suggest that neural responses to infant stimuli involve brain regions that process rewards. However, these studies have yet to investigate individual differences in tendencies to engage or withdraw from motivationally relevant stimuli. To investigate this, we used event-related fMRI to scan 17 nulliparous women. Participants were presented with novel infant cries of two distress levels (low and high) and unknown infant faces of varying affect (happy, sad, and neutral) in a randomized, counter-balanced order. Brain activation was subsequently correlated with scores on the Behavioral Inhibition System/Behavioral Activation System scale. Infant cries activated bilateral superior and middle temporal gyri (STG and MTG) and precentral and postcentral gyri. Activation was greater in bilateral temporal cortices for low- relative to high-distress cries. Happy relative to neutral faces activated the ventral striatum, caudate, ventromedial prefrontal, and orbitofrontal cortices. Sad versus neutral faces activated the precuneus, cuneus, and posterior cingulate cortex, and behavioral activation drive correlated with occipital cortical activations in this contrast. Behavioral inhibition correlated with activation in the right STG for high- and low-distress cries relative to pink noise. Behavioral drive correlated inversely with putamen, caudate, and thalamic activations for the comparison of high-distress cries to pink noise. Reward-responsiveness correlated with activation in the left precentral gyrus during the perception of low-distress cries relative to pink noise. Our findings indicate that infant cry stimuli elicit activations in areas implicated in auditory processing and social cognition. Happy infant faces may be encoded as rewarding, whereas sad faces activate regions associated with empathic processing. Differences in motivational tendencies may modulate neural responses to infant cues

Response Properties of Human Amygdala Subregions: Evidence Based on Functional MRI Combined with Probabilistic Anatomical Maps

The human amygdala is thought to play a pivotal role in the processing of emotionally significant sensory information. The major subdivisions of the human amygdala—the laterobasal group (LB), the superficial group (SF), and the centromedial group (CM)—have been anatomically delineated, but the functional response properties of these amygdala subregions in humans are still unclear. We combined functional MRI with cyto-architectonically defined probabilistic maps to analyze the response characteristics of amygdala subregions in subjects presented with auditory stimuli. We found positive auditory stimulation-related signal changes predominantly in probabilistically defined LB, and negative responses predominantly in SF and CM. In the left amygdala, mean response magnitude in the core area of LB with 90–100% assignment probability was significantly larger than in the core areas of SF and CM. These differences were observed for pleasant and unpleasant stimuli. Our findings reveal that the probabilistically defined anatomical subregions of the human amygdala show distinctive fMRI response patterns. The stronger auditory responses in LB as compared with SF and CM may reflect a predominance of auditory inputs to human LB, similar to many animal species in which the majority of sensory, including auditory, afferents project to this subdivision of the amygdala. Our study indicates that the intrinsic functional differentiation of the human amygdala may be probed using fMRI combined with probabilistic anatomical maps

Exploration of the Neural Correlates of Ticklish Laughter by Functional Magnetic Resonance Imaging

The burst of laughter that is evoked by tickling is a primitive form of vocalization. It evolves during an early phase of postnatal life and appears to be independent of higher cortical circuits. Clinicopathological observations have led to suspicions that the hypothalamus is directly involved in the production of laughter. In this functional magnetic resonance imaging investigation, healthy participants were 1) tickled on the sole of the right foot with permission to laugh, 2) tickled but asked to stifle laughter, and 3) requested to laugh voluntarily. Tickling that was accompanied by involuntary laughter activated regions in the lateral hypothalamus, parietal operculum, amygdala, and right cerebellum to a consistently greater degree than did the 2 other conditions. Activation of the periaqueductal gray matter was observed during voluntary and involuntary laughter but not when laughter was inhibited. The present findings indicate that hypothalamic activity plays a crucial role in evoking ticklish laughter in healthy individuals. The hypothalamus promotes innate behavioral reactions to stimuli and sends projections to the periaqueductal gray matter, which is itself an important integrative center for the control of vocalization. A comparison of our findings with published data relating to humorous laughter revealed the involvement of a common set of subcortical center

Toward a neuroscience of parenting : adult attachment and oxytocin affect neural and behavioral responses to infant attachment signals

As infants are fully dependent on their parents, correct perception and interpretation of infant signals is crucial for infant survival. It is therefore not surprising that specific brain circuits and neuroendocrine processes have evolved to perceive infant signals correctly and to respond adequately. However, parents vary in their ability to respond to their infants in a sensitive way and several factors may be involved in parental sensitive responsiveness. One important factor influencing parenting behavior is the neuropeptide oxytocin. Of all the hormones involved in parenting and other social behaviors, oxytocin has received the most interest, as evidenced by the high number of scientific studies over the past decade (Bos, Panksepp, Bluthé, & Honk, 2012; Van IJzendoorn & Bakermans-Kranenburg, 2012). Many studies suggest that oxytocin is related to sensitive parenting (Bakermans-Kranenburg & Van IJzendoorn, 2008; Feldman, Weller, Zagoory-Sharon, & Levine, 2007), although the exact mechanism underlying this positive association is not entirely clear yet. Another factor that influences parenting behavior is adult state of mind with respect to attachment (Van IJzendoorn, 1995). In the current dissertation, the role of oxytocin and adult attachment in parenting is examined with a series of functional magnetic resonance imaging experiments.LEI Universiteit LeidenDevelopment Psychopathology in context: famil