Functional connectivity of the human amygdala in health and in depression

To analyze the functioning of the amygdala in depression, we performed the first voxel-level resting state functional-connectivity neuroimaging analysis of depression of voxels in the amygdala with all other voxels in the brain, with 336 patients with major depressive disorder and 350 controls. Amygdala voxels had decreased functional connectivity with the orbitofrontal cortex, temporal lobe areas, including the temporal pole, inferior temporal gyrus, and the parahippocampal gyrus. The reductions in the strengths of the functional connectivity of the amygdala voxels with the medial orbitofrontal cortex and temporal lobe voxels were correlated with increases in the Beck Depression Inventory score and in the duration of illness measures of depression. Parcellation analysis in 350 healthy controls based on voxel-level functional connectivity showed that the basal division of the amygdala has high functional connectivity with medial orbitofrontal cortex areas, and the dorsolateral amygdala has strong functional connectivity with the lateral orbitofrontal cortex and related ventral parts of the inferior frontal gyrus. In depression, the basal amygdala division had especially reduced functional connectivity with the medial orbitofrontal cortex which is involved in reward; and the dorsolateral amygdala subdivision had relatively reduced functional connectivity with the lateral orbitofrontal cortex which is involved in non-reward

Neuron numbers increase in the human amygdala from birth to adulthood, but not in autism.

Remarkably little is known about the postnatal cellular development of the human amygdala. It plays a central role in mediating emotional behavior and has an unusually protracted development well into adulthood, increasing in size by 40% from youth to adulthood. Variation from this typical neurodevelopmental trajectory could have profound implications on normal emotional development. We report the results of a stereological analysis of the number of neurons in amygdala nuclei of 52 human brains ranging from 2 to 48 years of age [24 neurotypical and 28 autism spectrum disorder (ASD)]. In neurotypical development, the number of mature neurons in the basal and accessory basal nuclei increases from childhood to adulthood, coinciding with a decrease of immature neurons within the paralaminar nucleus. Individuals with ASD, in contrast, show an initial excess of amygdala neurons during childhood, followed by a reduction in adulthood across nuclei. We propose that there is a long-term contribution of mature neurons from the paralaminar nucleus to other nuclei of the neurotypical human amygdala and that this growth trajectory may be altered in ASD, potentially underlying the volumetric changes detected in ASD and other neurodevelopmental or neuropsychiatric disorders

Value Encoding in Single Neurons in the Human Amygdala during Decision Making

A growing consensus suggests that the brain makes simple choices by assigning values to the stimuli under consideration and then comparing these values to make a decision. However, the network involved in computing the values has not yet been fully characterized. Here, we investigated whether the human amygdala plays a role in the computation of stimulus values at the time of decision making. We recorded single neuron activity from the amygdala of awake patients while they made simple purchase decisions over food items. We found 16 amygdala neurons, located primarily in the basolateral nucleus that responded linearly to the values assigned to individual items

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

What does the amygdala contribute to social cognition?

The amygdala has received intense recent attention from neuroscientists investigating its function at the molecular, cellular, systems, cognitive, and clinical level. It clearly contributes to processing emotionally and socially relevant information, yet a unifying description and computational account have been lacking. The difficulty of tying together the various studies stems in part from the sheer diversity of approaches and species studied, in part from the amygdala's inherent heterogeneity in terms of its component nuclei, and in part because different investigators have simply been interested in different topics. Yet, a synthesis now seems close at hand in combining new results from social neuroscience with data from neuroeconomics and reward learning. The amygdala processes a psychological stimulus dimension related to saliency or relevance; mechanisms have been identified to link it to processing unpredictability; and insights from reward learning have situated it within a network of structures that include the prefrontal cortex and the ventral striatum in processing the current value of stimuli. These aspects help to clarify the amygdala's contributions to recognizing emotion from faces, to social behavior toward conspecifics, and to reward learning and instrumental behavior

Temporal precedence of emotion over attention modulations in the lateral amygdala: Intracranial ERP evidence from a patient with temporal lobe epilepsy

Previous fMRI studies have reported mixed evidence for the influence of selective attention on amygdala responses to emotional stimuli, with some studies showing "automatic" emotional effects to threat-related stimuli without attention (or even without awareness), but other studies showing a gating of amygdala activity by selective attention with no response to unattended stimuli. We recorded intracranial local field potentials from the intact left lateral amygdala in a human patient prior to surgery for epilepsy and tested, with a millisecond time resolution, for neural responses to fearful faces appearing at either task-relevant or task-irrelevant locations. Our results revealed an early emotional effect in the amygdala arising prior to, and independently of, attentional modulation. However, at a later latency, we found a significant modulation of the differential emotional response when attention was directed toward or away from fearful faces. These results suggest separate influences of emotion and attention on amygdala activation and may help reconcile previous discrepancies concerning the relative responsiveness of the human amygdala to emotional and attentional factors

Task modulation of single-neuron activity in the human amygdala and hippocampus

The human amygdala and hippocampus are critically involved in various processes in face perception. However, it remains unclear how task demands or evaluative contexts modulate processes underlying face perception. In this study, we employed two task instructions when participants viewed the same faces and recorded single-neuron activity from the human amygdala and hippocampus. We comprehensively analyzed task modulation for three key aspects of face processing and we found that neurons in the amygdala and hippocampus (1) encoded high-level social traits such as perceived facial trustworthiness and dominance and this response was modulated by task instructions; (2) encoded low-level facial features and demonstrated region-based feature coding, which was not modulated by task instructions; and (3) encoded fixations on salient face parts such as the eyes and mouth, which was not modulated by task instructions. Together, our results provide a comprehensive survey of task modulation of neural processes underlying face perception at the single-neuron level in the human amygdala and hippocampus

Fear, faces, and the human amygdala

The amygdala's historical role in processing stimuli related to threat and fear is being modified to suggest a role that is broader and more abstract. Amygdala lesions impair the ability to seek out and make use of the eye region of faces, resulting in impaired fear perception. Other studies in rats and humans revive earlier proposals that the amygdala is important not only for fear perception as such, but also for detecting saliency and biological relevance. Debates about some features of this processing now suggest that while the amygdala can process fearful facial expressions in the absence of conscious perception, and while there is some degree of preattentive processing, this depends on the context and is not necessarily more rapid than cortical processing routes. A large current research effort extends the amygdala's putative role to a number of psychiatric illnesses