Amygdala and auditory cortex exhibit distinct sensitivity to relevant acoustic features of auditory emotions

Abstract

Amygdala Temporal voice area Auditory emotions fMRI a b s t r a c tDiscriminating between auditory signals of different affective value is critical to successful social interaction. It is commonly held that acoustic decoding of such signals occurs in the auditory system, whereas affective decoding occurs in the amygdala. However, given that the amygdala receives direct subcortical projections that bypass the auditory cortex, it is possible that some acoustic decoding occurs in the amygdala as well, when the acoustic features are relevant for affective discrimination. We tested this hypothesis by combining functional neuroimaging with the neurophysiological phenomena of repetition suppression (RS) and repetition enhancement (RE) in human listeners. Our results show that both amygdala and auditory cortex responded differentially to physical voice features, suggesting that the amygdala and auditory cortex decode the affective quality of the voice not only by processing the emotional content from previously processed acoustic features, but also by processing the acoustic features themselves, when these are relevant to the identification of the voice's affective value. Specifically, we found that the auditory cortex is sensitive to spectral high-frequency voice cues when discriminating vocal anger from vocal fear and joy, whereas the amygdala is sensitive to vocal pitch when discriminating between negative vocal emotions (i.e., anger and fear). Vocal pitch is an instantaneously recognized voice feature, which is potentially transferred to the amygdala by direct subcortical projections. These results together provide evidence that, besides the auditory cortex, the amygdala too processes acoustic information, when this is relevant to the discrimination of auditory emotions.© 2016 Elsevier Ltd. All rights reserved. Available online at www.sciencedirect.com ScienceDirectJournal homepage: www.elsevier.com/locate/cortex c o r t e x 8 5 ( 2 0 1 6 ) 1 1 6 e1 2 5http://dx

Music-listening regulates human microRNA transcriptome

“…These are in agreement with previous reports of brain plasticity and improved cognitive functions like learning, verbal ability and memory after music exposure and training [72][73][74][75]. Acoustic stimuli from music-listening induce neural spike patterns which are transduced via the auditory pathway within milliseconds [76][77][78] and evoke emotions in the limbic system [79]. At the molecular level, neural stimulation is conducted via calcium channel activity and neurotransmitters, which activate immediate early genes (IEG) thereby regulating gene and microRNA expression patterns [80][81][82][83].…”

Neurocognitive processing efficiency for non-alarm rather than alarm signaling in human scream calls

“…We assumed that the human brain might process alarm screams with significant efficiency compared with non-alarm screams as quantified by the level of neural signals in [1] and the connectivity between brain areas that are central to affective sound processing [22,27]. Voice signals and affect bursts are usually processed in a distributed brain network, consisting of the auditory cortex, the amygdala, and the inferior frontal cortex (IFC) [1,22,28], which provide an acoustic and socio-affective analysis of these signals [29,30], respectively. To identify the neural dynamics of scream call processing in this network, we asked humans to listen to the same selected 84 screams as in experiments 2 and 3.…”

A neurocognitive model of perceptual decision‐making on emotional signals

“…The emotion-matching paradigm also strongly recruited the bilateral amygdala. Generally thought of as a module of automatic detection of emotions (Frühholz & Grandjean, 2013a;Öhman, 2002;Pannese et al, 2015Pannese et al, , 2016Phelps & LeDoux, 2005;Vuilleumier, Armony, Driver, & Dolan, 2001), the amygdala is preferentially recruited by angry and fearful faces (Adams, Gordon, Baird, Ambady, & Kleck, 2003;Milesi et al, 2014;Phelps et al, 2001;Repeiski, Smith, Sansom, & Repetski, 1996), which are the predominant stimuli in the emotion-matching paradigm. However, an alternative role for involvement of the amygdala is not as an automatic detector of emotions per se, but rather as a detector of relevant and salient stimuli, of which emotional expressions represent a subclass (Sander et al, 2003).…”

“…For example, the procedure of fear conditioning instills an initially neutral stimulus with the capacity of inducing reactions and behaviors that are biologically relevant (e.g., freezing or fleeing) upon consistent association with an aversive unconditioned stimulus (Pape & Pare, 2010). Furthermore, the amygdala is likely to process diverse emotional expressions, such as facial expressions (Haxby, Hoffman, & Gobbini, 2002;O'Toole, Roark, & Abdi, 2002;Rossion, 2015;Sabatinelli et al, 2011) and vocal prosody features (Fruhholz, Klaas, Patel, & Grandjean, 2015;Frühholz et al, 2015Frühholz et al, , 2016Pannese, Grandjean, & Frühholz, 2015, Pannese et al, 2016 as relevant social signals (Sander et al, 2003). The large variety of cortical and subcortical projections to and from the amygdala provide it with information about the properties of the stimulus as well as the ongoing goals and needs of the organism (J. L. Price, 2003).…”