Primary auditory cortex representation of fear‐conditioned musical sounds

Abstract

Auditory cortex is required for discriminative fear conditioning beyond the classical amygdala microcircuit, but its precise role is unknown. It has previously been suggested that Heschl's gyrus, which includes primary auditory cortex (A1), but also other auditory areas, encodes threat predictions during presentation of conditioned stimuli (CS) consisting of monophones, or frequency sweeps. The latter resemble natural prosody and contain discriminative spectro-temporal information. Here, we use functional magnetic resonance imaging (fMRI) in humans to address CS encoding in A1 for stimuli that contain only spectral but no temporal discriminative information.Two musical chords (complex) or two monophone tones (simple) were presented in a signaled reinforcement context (reinforced CS+ and nonreinforced CS−), or in a different context without reinforcement (neutral sounds, NS1 and NS2), with an incidental sound detection task. CS/US association encoding was quantified by the increased discriminability of BOLD patterns evoked by CS+/CS−, compared to NS pairs with similar physical stimulus differences and task demands. A1 was defined on a single-participant level and based on individual anatomy. We find that in A1, discriminability of CS+/CS− was higher than for NS1/NS2. This representation of unconditioned stimulus (US) prediction was of comparable magnitude for both types of sounds. We did not observe such encoding outside A1. Different from frequency sweeps investigated previously, musical chords did not share representations of US prediction with monophone sounds. To summarize, our findings suggest decodable representation of US predictions in A1, for various types of CS, including musical chords that contain no temporal discriminative information.associative learning, discriminative fear conditioning, emotional learning, multivariate pattern analysis, spectrotemporal information, threat conditioning, threat representation

Transcranial theta-burst stimulation of primary sensory cortex attenuates somatosensory threat memory in humans

“…However, we did not find clear evidence that the role of S1 in threat conditioning and threat-memory retention differed between simple and complex somatosensory stimuli (here differentiated by the temporal pattern of the stimulus across one or two fingers). On the other hand, our findings are in line with human neuroimaging studies that found equal CS+/CS-neural pattern discriminability for simple and complex CS in the auditory cortex 34,35 and that were able to cross-decode simple CS threat predictions from complex threat predictions and vice versa 34 . However, it is possible that experiments with larger sample sizes may yet detect such complexity effects 62,63 .…”

“…In human studies, threat-predictive CS+ and safe CS− elicit differential evoked-potential amplitude, oscillatory synchrony, and univariate fMRI BOLD amplitude in visual cortex [29][30][31] , multivariate BOLD patterns in olfactory cortex 32 , and univariate BOLD amplitude as well as multivariate patterns in the auditory cortex, with no difference between simple and complex CS [33][34][35] .…”

Activation in human auditory cortex in relation to the loudness and unpleasantness of low-frequency and infrasound stimuli

“…It is of course theoretically possible for a listener to develop a learned aversion for previously neutral sounds (as a result of past events), which might ultimately lead to elevated unpleasantness when exposed to these sounds. Findings from research in mice [21] and human listeners [22] suggest that such a learned aversive valence for acoustic signals may then be reflected by neural responses in the AC. Given that activation in AC was not better explained by unpleasantness relative to the other two variables in the present study, though, our data do not support the idea that learned aversion played an important role with respect to listeners' unpleasantness ratings.…”

“…20]. Other studies suggest that a learned aversive valence for sounds (e.g., through fear conditioning), which might be the cause of a higher unpleasantness in some cases, is reflected by altered AC activity [e.g., 21,22]. Given that activation in response to LFS and IS appears to be very similar to that of typical audio sound, we hypothesized that fMRI is a suitable tool to disentangle the representation of loudness and unpleasantness and to identify interindividual differences in the perception of LFS and IS.…”

Asymmetric representation of aversive prediction errors in Pavlovian threat conditioning

“…Multivariate analysis of high-resolution fMRI might be more appropriate to delineate such representations [43][44][45] . Table 1).…”