Clinical outcome of selective amygdalectomy in a series of patients with resistant temporal lobe epilepsy

Background: Selective amygdalohippocampectomy is one of the main approaches for treating medial temporal lobe epilepsy (TLE). We herewith describe seven cases of amygdala lesions treated with selective amygdalectomy with the hippocampus saving procedure. Furthermore, we explain the trans-middle temporal gyrus transventricular approach for selective amygdalectomy. Methods: We studied patients with TLE who underwent selective amygdalectomy with hippocampal saving procedure between March 2012 and July 2018. We preferred the trans-middle temporal gyrus transventricular approach. We adopted pterional craniotomy with extensive exposure of the base and posterior of the temporal lobe. The posterior margin of resection in the intraventricular part of the amygdala was considered the inferior choroidal point. Medially anterior part of the uncus was resected until reaching the ambient cistern. We applied the transcortical transventricular approach for selective amygdalectomy in all patients. Results: We present 11 cases having an amygdala lesion in our series, seven of whom underwent selective amygdalectomy with hippocampal sparing. Nine patients had neoplastic lesions, and in two of them, gliosis was evident. Total resection of the lesion was achieved in all cases based on postoperative magnetic resonance imaging. No unusual complication or surgically-related new neurological deficit occurred. Conclusion: We consider the resection of the amygdala until the inferior choroidal point sufficient for the disconnection of its circuits, which results in more effective control of seizures and reduction of surgery time and complications.

Interaction between decision-making and interoceptive representations of bodily arousal in frontal cortex

Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted “U” relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded and used as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased, and the relationship between HR and RTs was altered. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a population-coding analysis, we show that after bilateral amygdala lesions, the balance of encoding in dACC is skewed away from signaling either reward value or choice direction toward HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex.

Impairment of emotional expression detection after unilateral amygdala resection

Detecting facial emotional expressions is an initial and indispensable for face-to-face communication. Neuropsychological studies on the neural substrates of this process have shown that bilateral amygdala lesions impaired the detection of emotional facial expressions. However, the findings were inconsistent, possibly due to the limited number of patients examined. Furthermore, this processing is based on emotional or visual factors of facial expressions remains unknown. To investigate this issue, we tested the group of patients (n = 23) with unilateral resection of anterior temporal lobe structures, including the amygdala, and compared their performance under resected and intact hemisphere stimulation conditions. The patients were asked to detect normal facial expressions of anger and happiness, and artificially created anti-expressions, among a crowd with neutral expressions. Reaction times were shorter to detect normal versus anti-expressions when the target faces were presented to the contralateral visual field (i.e., stimulation of the intact hemisphere) than to the ipsilateral visual field (i.e., stimulation of the resected hemisphere). Our findings suggest that the amygdala plays an essential role in the detection of emotional facial expressions, according to the emotional significance of the expressions.

Toward a neuropsychology of political orientation: exploring ideology in patients with frontal and midbrain lesions

How do people form their political beliefs? In an effort to address this question, we adopt a neuropsychological approach. In a natural experiment, we explored links between neuroanatomy and ideological preferences in two samples of brain lesion patients in New York City. Specifically, we compared the political orientations of patients with frontal lobe lesions, patients with amygdala lesions and healthy control subjects. Lesion type classification analyses revealed that people with frontal lesions held more conservative (or less liberal) beliefs than those with anterior temporal lobe lesions or no lesions. Additional analyses predicting ideology by extent of damage provided convergent evidence that greater damage in the dorsolateral prefrontal cortex—but not the amygdala—was associated with greater conservatism. These findings were robust to model specifications that adjusted for demographic, mood, and affect-related variables. Although measures of executive function failed to mediate the relationship between frontal lesions and ideology, our findings suggest that the prefrontal cortex may play a role in promoting the development of liberal ideology. Our approach suggests useful directions for future work to address the issue of whether biological developments precede political attitudes or vice versa —or both. This article is part of the theme issue ‘The political brain: neurocognitive and computational mechanisms’.

Interaction between decision-making and interoceptive representations of bodily arousal in frontal cortex

Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted ‘U’ relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased and the relationship between HR and RTs was reversed. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a novel population-coding analysis, we show that bilateral amygdala lesions skew the balance of encoding in dACC away from signaling either reward value or choice direction towards HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex. Our findings may shed light on the neural mechanisms underlying some psychiatric disorders linked to amygdala dysfunction that are characterized by heightened arousal and deficits in decision-making.Significance statementHow bodily arousal states influence decision-making has been a central question in psychology, but the neural mechanisms are unclear. We recorded heart rate, a measure of bodily arousal, while simultaneously monitoring neural activity in orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaques making reward-guided decisions. In intact macaques higher HR was associated with shorter reaction times. Concurrently, the activity of a set of neurons in OFC and dACC selectively encoded HR. Following amygdala lesions, HR generally increased and now the relationship between HR and reaction times was reversed. At the neural level, the balance of encoding in dACC shifted towards signaling HR, suggesting a specific mechanism through which arousal influences decision-making.

Bilateral amygdala damage linked to impaired ability to predict others' fear but preserved moral judgements about causing others fear

The amygdala is a subcortical structure implicated in both the expression of conditioned fear and social fear recognition. Social fear recognition deficits following amygdala lesions are often interpreted as reflecting perceptual deficits, or the amygdala's role in coordinating responses to threats. But these explanations fail to capture why amygdala lesions impair both physiological and behavioural responses to multimodal fear cues and the ability to identify them. We hypothesized that social fear recognition deficits following amygdala damage reflect impaired conceptual understanding of fear. Supporting this prediction, we found specific impairments in the ability to predict others' fear (but not other emotions) from written scenarios following bilateral amygdala lesions. This finding is consistent with the suggestion that social fear recognition, much like social recognition of states like pain, relies on shared internal representations. Preserved judgements about the permissibility of causing others fear confirms suggestions that social emotion recognition and morality are dissociable.

Effects of Amygdala Lesions on Object-Based Versus Action-Based Learning in Macaques

The neural systems that underlie reinforcement learning (RL) allow animals to adapt to changes in their environment. In the present study, we examined the hypothesis that the amygdala would have a preferential role in learning the values of visual objects. We compared a group of monkeys (Macaca mulatta) with amygdala lesions to a group of unoperated controls on a two-armed bandit reversal learning task. The task had two conditions. In the What condition, the animals had to learn to select a visual object, independent of its location. And in the Where condition, the animals had to learn to saccade to a location, independent of the object at the location. In both conditions choice-outcome mappings reversed in the middle of the block. We found that monkeys with amygdala lesions had learning deficits in both conditions. Monkeys with amygdala lesions did not have deficits in learning to reverse choice-outcome mappings. Rather, amygdala lesions caused the monkeys to become overly sensitive to negative feedback which impaired their ability to consistently select the more highly valued action or object. These results imply that the amygdala is generally necessary for RL.

Cross-species convergence in pupillary response: understanding human anxiety via non-human primate amygdala lesion

Few studies have used matched affective paradigms to compare humans and non-human primates. In monkeys with amygdala lesions and youth with anxiety disorders, we examined cross-species pupillary responses during a saccade-based, affective attentional capture task. Given evidence of enhanced amygdala function in anxiety, we hypothesized that opposite patterns would emerge in lesioned monkeys and anxious participants. A total of 53 unmedicated youths (27 anxious, 26 healthy) and 8 adult male rhesus monkeys (Macaca mulatta) completed matched behavioral paradigms. Four monkeys received bilateral excitotoxic amygdala lesions and four served as unoperated controls. Compared to healthy youth, anxious youth exhibited increased pupillary constriction in response to emotional and non-emotional distractors (F(1,48) = 6.28, P = 0.02, η2p = 0.12). Pupillary response was associated significantly with anxiety symptoms severity (F(1,48) = 5.59, P = 0.02, η2p = 0.10). As hypothesized, lesioned monkeys exhibited the opposite pattern i.e. decreased pupillary constriction in response to distractors, compared to unoperated control monkeys (F(1,32) = 24.22, P < 0.001, η2 = 0.33). Amygdala lesioned monkeys and youth with anxiety disorders show opposite patterns of pupil constriction in the context of an affective distractor task. Such findings suggest the presence of altered amygdala circuitry functioning in anxiety. Future lesion and human neuroimaging work might examine the way in which specific amygdala sub-nuclei and downstream circuits mediate these effects.