Uncovering the functional anatomy of the human insula during speech
Abstract
The contribution of insular cortex to speech production remains unclear and controversial given diverse findings from functional neuroimaging and lesional data. To create a precise spatiotemporal map of insular activity, we performed a series of experiments: single-word articulations of varying complexity, non-speech orofacial movements and speech listening, in a cohort of 27 patients implanted with penetrating intracranial electrodes. The posterior insula was robustly active bilaterally, but after the onset of articulation, during listening to speech and during production of non-speech mouth movements. Preceding articulation there was very sparse activity, localized primarily to the frontal operculum rather than the insula. Posterior insular was active coincident with superior temporal gyrus, but was more active for self-generated speech than external speech, the opposite of the superior temporal gyrus. These findings support the conclusion that the insula does not serve pre-articulatory preparatory roles.
Data availability
Source data files and a MATLAB plotting function have been provided for Figures 2, 3, 5 and 6.
Article and author information
Author details
Funding
National Institute on Deafness and Other Communication Disorders (DC014589)
- Oscar Woolnough
- Kiefer James Forseth
- Patrick Sarahan Rollo
- Nitin Tandon
National Institute of Neurological Disorders and Stroke (NS098981)
- Oscar Woolnough
- Kiefer James Forseth
- Patrick Sarahan Rollo
- Nitin Tandon
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Patients participated in the experiments after written informed consent was obtained. All experimental procedures were reviewed and approved by the Committee for the Protection of Human Subjects (CPHS) of the University of Texas Health Science Center at Houston as Protocol Number: HSC-MS-06-0385
Reviewing Editor
- Barbara G Shinn-Cunningham, Carnegie Mellon University, United States
Version history
- Received: October 27, 2019
- Accepted: December 12, 2019
- Accepted Manuscript published: December 19, 2019 (version 1)
- Version of Record published: January 3, 2020 (version 2)
Copyright
© 2019, Woolnough et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
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- Genetics and Genomics
- Neuroscience
In the fruit fly Drosophila melanogaster, gustatory sensory neurons express taste receptors that are tuned to distinct groups of chemicals, thereby activating neural ensembles that elicit either feeding or avoidance behavior. Members of a family of ligand -gated receptor channels, the Gustatory receptors (Grs), play a central role in these behaviors. In general, closely related, evolutionarily conserved Gr proteins are co-expressed in the same type of taste neurons, tuned to chemically related compounds, and therefore triggering the same behavioral response. Here, we report that members of the Gr28 subfamily are expressed in largely non-overlapping sets of taste neurons in Drosophila larvae, detect chemicals of different valence, and trigger opposing feeding behaviors. We determined the intrinsic properties of Gr28 neurons by expressing the mammalian Vanilloid Receptor 1 (VR1), which is activated by capsaicin, a chemical to which wild-type Drosophila larvae do not respond. When VR1 is expressed in Gr28a neurons, larvae become attracted to capsaicin, consistent with reports showing that Gr28a itself encodes a receptor for nutritious RNA. In contrast, expression of VR1 in two pairs of Gr28b.c neurons triggers avoidance to capsaicin. Moreover, neuronal inactivation experiments show that the Gr28b.c neurons are necessary for avoidance of several bitter compounds. Lastly, behavioral experiments of Gr28 deficient larvae and live Ca2+ imaging studies of Gr28b.c neurons revealed that denatonium benzoate, a synthetic bitter compound that shares structural similarities with natural bitter chemicals, is a ligand for a receptor complex containing a Gr28b.c or Gr28b.a subunit. Thus, the Gr28 proteins, which have been evolutionarily conserved over 260 million years in insects, represent the first taste receptor subfamily in which specific members mediate behavior with opposite valence.