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Noradrenaline tracks emotional modulation of attention in human amygdala.

ABSTRACT: The noradrenaline (NA) system is one of the brain's major neuromodulatory systems; it originates in a small midbrain nucleus, the locus coeruleus (LC), and projects widely throughout the brain.¹^,² The LC-NA system is believed to regulate arousal and attention³^,⁴ and is a pharmacological target in multiple clinical conditions.⁵^,⁶^,⁷ Yet our understanding of its role in health and disease has been impeded by a lack of direct recordings in humans. Here, we address this problem by showing that electrochemical estimates of sub-second NA dynamics can be obtained using clinical depth electrodes implanted for epilepsy monitoring. We made these recordings in the amygdala, an evolutionarily ancient structure that supports emotional processing⁸^,⁹ and receives dense LC-NA projections,¹⁰ while patients (n = 3) performed a visual affective oddball task. The task was designed to induce different cognitive states, with the oddball stimuli involving emotionally evocative images,¹¹ which varied in terms of arousal (low versus high) and valence (negative versus positive). Consistent with theory, the NA estimates tracked the emotional modulation of attention, with a stronger oddball response in a high-arousal state. Parallel estimates of pupil dilation, a common behavioral proxy for LC-NA activity,¹² supported a hypothesis that pupil-NA coupling changes with cognitive state,¹³^,¹⁴ with the pupil and NA estimates being positively correlated for oddball stimuli in a high-arousal but not a low-arousal state. Our study provides proof of concept that neuromodulator monitoring is now possible using depth electrodes in standard clinical use.

SUBMITTER: Bang D

PROVIDER: S-EPMC10957395 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Noradrenaline tracks emotional modulation of attention in human amygdala.

Bang Dan D Luo Yi Y Barbosa Leonardo S LS Batten Seth R SR Hadj-Amar Beniamino B Twomey Thomas T Melville Natalie N White Jason P JP Torres Alexis A Celaya Xavier X Ramaiah Priya P McClure Samuel M SM Brewer Gene A GA Bina Robert W RW Lohrenz Terry T Casas Brooks B Chiu Pearl H PH Vannucci Marina M Kishida Kenneth T KT Witcher Mark R MR Montague P Read PR

Current biology : CB 20231023 22

The noradrenaline (NA) system is one of the brain's major neuromodulatory systems; it originates in a small midbrain nucleus, the locus coeruleus (LC), and projects widely throughout the brain.1,2 The LC-NA system is believed to regulate arousal and attention3,4 and is a pharmacological target in multiple clinical conditions.5,6,7 Yet our understanding of its role in health an ...[more]

PMID: 37875110

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Project description:The amygdala is a key structure mediating emotional processing. Few studies have used direct electrical stimulation of the amygdala in humans to examine stimulation-elicited physiological and emotional responses, and the nature of such effects remains unclear. Determining the effects of electrical stimulation of the amygdala has important theoretical implications for current discrete and dimensional neurobiological theories of emotion, which differ substantially in their predictions about the emotional effects of such stimulation. To examine the effects of amygdala stimulation on physiological and subjective emotional responses we examined epilepsy patients undergoing intracranial EEG monitoring in which depth electrodes were implanted unilaterally or bilaterally in the amygdala. Nine subjects underwent both sham and acute monopolar electrical stimulation at various parameters in electrode contacts located in amygdala and within lateral temporal cortex control locations. Stimulation was applied at either 50 Hz or 130 Hz, while amplitudes were increased stepwise from 1 to 12 V, with subjects blinded to stimulation condition. Electrodermal activity (EDA), heart rate (HR), and respiratory rate (RR) were simultaneously recorded and subjective emotional response was probed after each stimulation period. Amygdala stimulation (but not lateral control or sham stimulation) elicited immediate and substantial dose-dependent increases in EDA and decelerations of HR, generally without affecting RR. Stimulation elicited subjective emotional responses only rarely, and did not elicit clinical seizures in any subject. These physiological results parallel stimulation findings with animals and are consistent with orienting/defensive responses observed with aversive visual stimuli in humans. In summary, these findings suggest that acute amygdala stimulation in humans can be safe and can reliably elicit changes in emotion physiology without significantly affecting subjective emotional experience, providing a useful approach for investigation of amygdala-mediated modulatory effects on cognition.

Dataset Information

Noradrenaline tracks emotional modulation of attention in human amygdala.

Publications

Noradrenaline tracks emotional modulation of attention in human amygdala.

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