Voice experiments in people with epilepsy have helped trace the circuit of electrical signals in the brain that allow its hearing center to sort out background sounds from their own voices.
Such auditory corollary discharge signals start and end in two subregions of the brain's top folded surface, or cortex, a new study shows. One large part of the cortex, the motor cortex, is known to control the body's voluntary muscle movements, including those involved in speech, while another large section, the auditory cortex, is known to control hearing.
In terms of evolution, the ability of animals and humans to tell one's own calls or voices from those of others is thought to have enabled threat perception and enhanced survival. The back-and-forth, milliseconds-long electrical signals that let the brain downplay background sounds are present, for instance, as crickets rapidly tell apart their own mating chirps from the chirps of others, as songbirds sing mating songs, and as bats use reverberations of sound to negotiate their environments.
In humans, disruptions to this system are also thought to be hallmarks of auditory hallucinations, or "hearing voices," in people with schizophrenia who cannot distinguish "real" voices from outside sounds, say the study authors. Disturbances in auditory corollary discharge signals are also thought to be involved in stuttering.
While previous experiments had tracked this electrical brain circuit to the motor cortex in mammals, the field has struggled to determine where discharge signals originate in the human motor cortex. This is partly because of the difficulty in recording brain activity while people are awake and talking, but mainly due to complexity of the computer analysis needed to analyze the recordings.
For the new study, led by researchers at NYU Langone Health, its Neuroscience Institute, and at NYU's Tandon School of Engineering, neuroscientists conducted voice experiments in eight adults with epilepsy. All were undergoing routine surgery to determine the source of their seizures and volunteered to participate in word exercises.
Publishing in the Proceedings of the National Academy of Sciences (PNAS) online Dec. 3, the report describes how the researchers mapped auditory corollary discharge signals from the bottom, or ventral, part of the motor cortex, a subregion called the precentral gyrus. The electrical signals, lasting on average 120 milliseconds, were then found to move down and across the folds of the precentral gyrus to a neighboring auditory cortical subregion, called the superior temporal gyrus.
"We believe our study solves a long-standing puzzle in our understanding of human speech, offering the first direct evidence of the motor cortex brain circuits involved in corollary discharge that allow us to stay alert to our surroundings even while we are speaking," said study lead investigator Amirhossein Khalilian-Gourtani, PhD. Khalilian-Gourtani is a postdoctoral research fellow in the Department of Neurology at NYU Grossman School of Medicine.
"Our findings also provide specific insight into schizophrenia, offering an explanation for the source of auditory hallucinations, as resulting from disrupted corollary discharge between the brain's motor and auditory cortices," said neuroscientist Adeen Flinker, PhD, study senior investigator.
"What we and many other researchers suspect is happening in some people with schizophrenia is that they are unable to dissociate their own voice from others or even other external stimuli," said Flinker, an associate professor in the Department of Neurology at NYU Grossman School of Medicine and NYU Tandon School of Engineering.
As part of the new study, researchers made more than 3,200 recordings of electrical brain activity while patients completed a series of voice experiments during planned breaks in their surgery. All patients had upward of 200 probes inserted into their brains to primarily monitor any seizure-related electrical activity. The research team then used a computer model to assess and predict what regions were active in the corollary discharge during speech in the word experiments designed to track the discharge.
Among the exercises, patients were asked to listen to and then repeat a word, such as "balloon;" complete a sentence with the same word when answering the question "The boy blew up a…?" and look at a picture of a balloon and describe it with the same word.
Each test required the patient to tune out what word they were hearing while still being alert to their visual and acoustic surroundings, staying focused and saying aloud the same word.
Study participants were mostly men and women in their 30s and 40s and were recorded since 2019 at NYU Langone. Researchers recorded electrical activity inside most subregions of the patients' brains as the patients heard themselves responding to recordings of statements being read aloud by others. Such audio-feedback tests have been developed to safely study how the human brain learns and processes speech.
Flinker says the team plans tests to assess further how and whether the corollary discharge circuit is active immediately before hallucinations induced during brain stimulation. They also have plans to work with psychiatrists on noninvasive means of testing the signal in people with schizophrenia.
Funding support for the study was provided by National Science Foundation grant HS-1912286 and National Institutes of Health grants R01NS109367 and R01NS115929.
Besides Khalilian-Gourtani and Flinker, other NYU Langone and NYU Tandon researchers involved in the study are co-investigators Ran Wang, Xupeng Chen, Leyao Yu, Patricia Dugan, Daniel Friedman, Werner Doyle, Orrin Devinsky, and Yao Wang.
