Abstract
BackgroundMultiple lines of evidence show that the human amygdala is part of a neural network important for perception of emotion from environmental stimuli, including for processing of intrinsic attractiveness/“goodness” or averseness/“badness,” i.e., affective valence.Objective/HypothesisWith this in mind, we investigated the effect of electrical brain stimulation of the human amygdala on perception of affective valence of images taken from the International Affective Picture Set (IAPS).MethodsUsing intracranial electrodes in patients with epilepsy, we first obtained event-related potentials (ERPs) in eight patients as they viewed IAPS images of varying affective valence. Next, in a further cohort of 10 patients (five female and five male), we measured the effect of 50 Hz electrical stimulation of the left amygdala on perception of affective valence from IAPS images.ResultsWe recorded distinct ERPs from the left amygdala and found significant differences in the responses between positively and negatively valenced stimuli (p = 0.002), and between neutral and negatively valenced stimuli (p = 0.017) 300–500 ms after stimulus onset. Next, we found that amygdala stimulation did not significantly affect how patients perceived valence for neutral images (p = 0.58), whereas stimulation induced patients to report both positively (p = 0.05) and negatively (< 0.01) valenced images as more neutral.ConclusionThese results render further evidence that the left amygdala participates in a neural network for perception of emotion from environmental stimuli. These findings support the idea that electrical stimulation disrupts this network and leads to partial disruption of perception of emotion. Harnessing this effect may have clinical implications in treatment of certain neuropsychiatric disorders using deep brain stimulation (DBS) and neuromodulation.
Highlights
One of the most extensively studied regions in the human brain with respect to anatomy and function is the amygdala (McDonald, 1998; Murray, 2007; Benarroch, 2015; Janak and Tye, 2015)
The task was designed de novo for the purpose of this study (Figure 1). 48 images were selected from the International Affective Picture System (IAPS) (Bradley and Lang, 2007) using the following criteria: images of scenes with people only, normal control affective valence values between 2 and 8 (1 and 9 were excluded due to extreme nature of some images)
We selected channels located within the left amygdala, hippocampus, and ventromedial prefrontal cortex, resulting in 39 electrodes in amygdala, 81 electrodes in hippocampus and 49 electrodes in vmPFC
Summary
One of the most extensively studied regions in the human brain with respect to anatomy and function is the amygdala (McDonald, 1998; Murray, 2007; Benarroch, 2015; Janak and Tye, 2015). Extensive evidence from non-human and human animal studies implicates the amygdala in a wide variety of cognitive functions, including for identifying emotional information from the environment (LaBar et al, 1998; Tye and Janak, 2007; FusarPoli et al, 2009; Salzman and Fusi, 2010). Functional MR studies in normal human subjects show amygdala activation during valence judgments (Canli et al, 2000; Garavan et al, 2001; Hariri et al, 2002; Phelps and LeDoux, 2005; Sergerie et al, 2008; Ball et al, 2009; Salzman and Fusi, 2010; Murray et al, 2014). Multiple lines of evidence show that the human amygdala is part of a neural network important for perception of emotion from environmental stimuli, including for processing of intrinsic attractiveness/“goodness” or averseness/“badness,” i.e., affective valence
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