The definitive version of this post was originally published on September 6, 2015 on the PLOS Neuroscience Community website, where I serve as an editor.
The tone of this post and the interview are a little different from my usual pieces. Heartfelt thanks to Luc Arnal, who went out of his way to answer my questions, serious and otherwise!
Luc Arnal, a post-doctoral scientist in David Poeppel’s laboratory at New York University, was having his brain hijacked. No, this isn’t a report of futuristic brain implants and neurohacking: rather, Arnal was experiencing the joys of fatherhood, together with the unavoidable alarm at hearing his newborn baby scream. Ever the scientist, he decided to explore what made those screams such an irresistible alarm signal. The answer fits in one word: roughness. Arnal applied an innovative approach to unpack the acoustic properties of screams along the two dimensions that characterize all sounds: time (how a sound evolves through time) and frequency (the pitch of a sound, among others, depends on its frequency). He found that alarm signals exploit a portion of the acoustic space that other sounds, such as normal voices, do not use: this part of the spectrum corresponds to our perception of roughness (think of how a heavily distorted guitar sounds, for instance, as opposed to a pure piano note). He then went on to characterize how our brains respond to alarm signals, and discovered that rough sounds selectively activate the amygdala, one of the structures in the brain that process emotions. Arnal and colleagues’ findings were recently published in Current Biology. Here, he went out of his way to answer questions, serious and otherwise, about his research.
Where did you find that idea of studying screams? Who among the authors is the horror movie buff? Did you create a “scream scale” to rate the most famous screams in Hollywood history by roughness?
I started being interested in screams because my newborn’s screams were literally hijacking my brain and I wondered what makes screams so efficient as an alarm signal. Interestingly, screams are highly relevant biologically: screaming is innate in humans and it constitutes a primordial vocalization that is possibly shared by various animals.
So I decided to characterize the acoustics of human screams. I wanted to analyze good scream recordings. Before recording volunteer screamers on a roller-coaster or in the lab I needed some preliminary evidence supporting my theory. I started working on excerpts from horror movies that were available on Youtube. But to be honest I’m not really a horror movie buff and it’s been really brutal and depressing for me to listen and edit so many screams overnight. But in the end, a few nightmares were totally worth the findings and the potential applications. A scream scale? We haven’t thought about that, but great idea to cast more credible victims for movies!
More seriously, you show that roughness is the defining characteristic of “alarm” signals, and that adding roughness to normal words makes them more fearsome, whereas filtering out the roughness makes screams more benign. Could you imagine a way that this filter would work in real time, in order to remove roughness in cases where it is unwanted (e.g. in economy class aboard planes)?
Well, filtering out rough modulations from the acoustic spectrum is a rather tricky manipulation especially in real time; we’re not there yet but I agree that ‘roughLess’ earplugs would be pretty amazing (although you’d probably miss the alarm signals if there is a real problem during your flight).
Also, you tested a series of sounds from musical instruments that were all considered “non-alarm” sounds. But did you try a very distorted guitar, like in hard rock or heavy metal (Black Sabbath comes to mind)?
We have compared alarm sounds with sounds from musical instruments played using Garage Band, but effects like distortion were not tested. On the other hand, we found that dissonant intervals sound rough (as do distorted guitars). It may sound counterintuitive that modern music (such as jazz and metal) uses these rough sounds that presumably trigger unpleasant, fearful responses in the brain. One possible explanation is that, in the same way that people enjoy being frightened and stimulating their amygdala when watching a horror movie, it is possible that roughness in music may induce slightly unpleasant and fearful responses in the brain of the listener, and maybe people who like hard rock music like it because it’s slightly aggressive and stimulating.
Even more seriously, your neuroimaging results suggest some specialization for the processing of screams and alarm sounds. Do we know of neurological disorders where the capacity to recognize danger through sounds is altered or abolished? Do the anatomical substrates of these disorders coincide with your fMRI findings?
Well yes, there are well-known cases of patients with bilateral lesions of the amygdala who have impaired perception of vocal affect, in particular of the expression of fear and anger. To our knowledge, however, no other work had found any acoustic specificity of the amygdalar response.
You show that alarm sounds activate the amygdala as well as the auditory cortex to a greater degree than non-danger sounds. Could you speculate on the neuronal pathways involved, especially with respect to the timing of their activation? In other words, would you think that the amygdala gets activated by alarm signals directly from subcortical structures, and then influences the amplitude of activity in the auditory cortex? Or, on the contrary, is the auditory cortex passing on information to the amygdala that then feeds the alarm detection signal back to auditory cortex?
This is a great question but we can only speculate about that since our fMRI data do not really allow investigating the timing of brain responses. Whether the recruitment of the amygdala by rough aversive sounds results from a direct routing from subcortical auditory nuclei to the amygdala or an indirect routing through the auditory cortex remains an open question. However, we think that our finding might support the view that fast temporally modulated (rough) sounds would be directly routed from subcortical auditory nuclei to the amygdala. The fact that the amygdala is activated by roughness regardless of context (vocal, musical) is consistent with this view. The fast recruitment of the amygdala might in turn cause sensory unpleasantness, increased attention or arousal, and speed up the reaction to the signaled danger. Importantly, this hypothesis does not rule out subsequent interactions with other cortical areas involved in the processing of more complex information (pertaining to the context or valence of the stimulus).
Arnal, L., Flinker, A., Kleinschmidt, A., Giraud, A., & Poeppel, D. (2015). Human Screams Occupy a Privileged Niche in the Communication Soundscape Current Biology, 25 (15), 2051-2056 DOI: 10.1016/j.cub.2015.06.043