Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation
Background: The exact architecture of the human auditory cortex remains a subject of debate, with discrepancies between functional and microstructural studies. In a hierarchical framework for sensory perception, simple sound perception is expected to take place in the primary auditory cortex, while...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-09-01
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| Series: | Brain Stimulation |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X22001802 |
| _version_ | 1811182539675533312 |
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| author | Chloé Jaroszynski Ricardo Amorim-Leite Pierre Deman Marcela Perrone-Bertolotti Florian Chabert Anne-Sophie Job-Chapron Lorella Minotti Dominique Hoffmann Olivier David Philippe Kahane |
| author_facet | Chloé Jaroszynski Ricardo Amorim-Leite Pierre Deman Marcela Perrone-Bertolotti Florian Chabert Anne-Sophie Job-Chapron Lorella Minotti Dominique Hoffmann Olivier David Philippe Kahane |
| author_sort | Chloé Jaroszynski |
| collection | DOAJ |
| description | Background: The exact architecture of the human auditory cortex remains a subject of debate, with discrepancies between functional and microstructural studies. In a hierarchical framework for sensory perception, simple sound perception is expected to take place in the primary auditory cortex, while the processing of complex, or more integrated perceptions is proposed to rely on associative and higher-order cortices. Objectives: We hypothesize that auditory symptoms induced by direct electrical stimulation (DES) offer a window into the architecture of the brain networks involved in auditory hallucinations and illusions. The intracranial recordings of these evoked perceptions of varying levels of integration provide the evidence to discuss the theoretical model. Methods: We analyzed SEEG recordings from 50 epileptic patients presenting auditory symptoms induced by DES. First, using the Juelich cytoarchitectonic parcellation, we quantified which regions induced auditory symptoms when stimulated (ROI approach). Then, for each evoked auditory symptom type (illusion or hallucination), we mapped the cortical networks showing concurrent high-frequency activity modulation (HFA approach). Results: Although on average, illusions were found more laterally and hallucinations more posteromedially in the temporal lobe, both perceptions were elicited in all levels of the sensory hierarchy, with mixed responses found in the overlap. The spatial range was larger for illusions, both in the ROI and HFA approaches. The limbic system was specific to the hallucinations network, and the inferior parietal lobule was specific to the illusions network. Discussion: Our results confirm a network-based organization underlying conscious sound perception, for both simple and complex components. While symptom localization is interesting from an epilepsy semiology perspective, the hallucination-specific modulation of the limbic system is particularly relevant to tinnitus and schizophrenia. |
| first_indexed | 2024-04-11T09:32:18Z |
| format | Article |
| id | doaj.art-6eef7d0bbf7240baa59ea1359a4d376a |
| institution | Directory Open Access Journal |
| issn | 1935-861X |
| language | English |
| last_indexed | 2024-04-11T09:32:18Z |
| publishDate | 2022-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj.art-6eef7d0bbf7240baa59ea1359a4d376a2022-12-22T04:31:49ZengElsevierBrain Stimulation1935-861X2022-09-0115510771087Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulationChloé Jaroszynski0Ricardo Amorim-Leite1Pierre Deman2Marcela Perrone-Bertolotti3Florian Chabert4Anne-Sophie Job-Chapron5Lorella Minotti6Dominique Hoffmann7Olivier David8Philippe Kahane9Univ. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, France; Corresponding author.Univ. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, FranceUniv. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, FranceUniv. Grenoble Alpes, CNRS, UMR5105, Laboratoire Psychologie et NeuroCognition, LPNC, 38000, Grenoble, FranceUniv. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, FranceUniv. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, FranceUniv. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, FranceUniv. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, FranceUniv. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, France; Aix Marseille Univ, Inserm, INS, Institut de Neurosciences des Systèmes, Marseille, France; Corresponding author. Univ. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, France.Univ. Grenoble Alpes, CHU Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN, 38000, Grenoble, France; Corresponding author.Background: The exact architecture of the human auditory cortex remains a subject of debate, with discrepancies between functional and microstructural studies. In a hierarchical framework for sensory perception, simple sound perception is expected to take place in the primary auditory cortex, while the processing of complex, or more integrated perceptions is proposed to rely on associative and higher-order cortices. Objectives: We hypothesize that auditory symptoms induced by direct electrical stimulation (DES) offer a window into the architecture of the brain networks involved in auditory hallucinations and illusions. The intracranial recordings of these evoked perceptions of varying levels of integration provide the evidence to discuss the theoretical model. Methods: We analyzed SEEG recordings from 50 epileptic patients presenting auditory symptoms induced by DES. First, using the Juelich cytoarchitectonic parcellation, we quantified which regions induced auditory symptoms when stimulated (ROI approach). Then, for each evoked auditory symptom type (illusion or hallucination), we mapped the cortical networks showing concurrent high-frequency activity modulation (HFA approach). Results: Although on average, illusions were found more laterally and hallucinations more posteromedially in the temporal lobe, both perceptions were elicited in all levels of the sensory hierarchy, with mixed responses found in the overlap. The spatial range was larger for illusions, both in the ROI and HFA approaches. The limbic system was specific to the hallucinations network, and the inferior parietal lobule was specific to the illusions network. Discussion: Our results confirm a network-based organization underlying conscious sound perception, for both simple and complex components. While symptom localization is interesting from an epilepsy semiology perspective, the hallucination-specific modulation of the limbic system is particularly relevant to tinnitus and schizophrenia.http://www.sciencedirect.com/science/article/pii/S1935861X22001802Auditory hallucination and illusionStereo-electroencephalographyDirect electrical stimulationGamma band activityProbabilistic brain mapping |
| spellingShingle | Chloé Jaroszynski Ricardo Amorim-Leite Pierre Deman Marcela Perrone-Bertolotti Florian Chabert Anne-Sophie Job-Chapron Lorella Minotti Dominique Hoffmann Olivier David Philippe Kahane Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation Brain Stimulation Auditory hallucination and illusion Stereo-electroencephalography Direct electrical stimulation Gamma band activity Probabilistic brain mapping |
| title | Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation |
| title_full | Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation |
| title_fullStr | Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation |
| title_full_unstemmed | Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation |
| title_short | Brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation |
| title_sort | brain mapping of auditory hallucinations and illusions induced by direct intracortical electrical stimulation |
| topic | Auditory hallucination and illusion Stereo-electroencephalography Direct electrical stimulation Gamma band activity Probabilistic brain mapping |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X22001802 |
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