Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activi...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-10-01
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| Series: | Frontiers in Human Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnhum.2021.737230/full |
| _version_ | 1818437641574547456 |
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| author | Kirill V. Nourski Kirill V. Nourski Mitchell Steinschneider Mitchell Steinschneider Ariane E. Rhone Rashmi N. Mueller Rashmi N. Mueller Hiroto Kawasaki Matthew I. Banks Matthew I. Banks |
| author_facet | Kirill V. Nourski Kirill V. Nourski Mitchell Steinschneider Mitchell Steinschneider Ariane E. Rhone Rashmi N. Mueller Rashmi N. Mueller Hiroto Kawasaki Matthew I. Banks Matthew I. Banks |
| author_sort | Kirill V. Nourski |
| collection | DOAJ |
| description | In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activity associated with predictable backgrounds and emphasizes detection of changes in the environment. In real life, the brain must resolve multiple unexpected sensory events occurring over different time scales. The local/global deviant experimental paradigm examines auditory predictive coding over multiple time scales. For short-term novelty [hundreds of milliseconds; local deviance (LD)], sequences of identical sounds (/xxxxx/) are interspersed with sequences that contain deviants (/xxxxy/). Long-term novelty [several seconds; global deviance (GD)] is created using either (a) frequent /xxxxx/ and infrequent /xxxxy/ sequences, or (b) frequent /xxxxy/ and infrequent /xxxxx/ sequences. In scenario (a), there is both an LD and a GD effect (LDGD, “double surprise”). In (b), the global deviant is a local standard, i.e., sequence of identical sounds (LSGD). Cortical responses reflecting LD and GD originate in different brain areas, have a different time course, and are differentially sensitive to general anesthesia. Neural processes underlying LD and GD have been shown to interact, reflecting overlapping networks subserving the detection of novel auditory stimuli. This study examined these interactions using intracranial electroencephalography in neurosurgical patients. Subjects performed a GD target detection task before and during induction of anesthesia with propofol. Recordings were made from the auditory cortex, surrounding auditory-related and prefrontal cortex in awake, sedated, and unresponsive states. High gamma activity was used to measure the neural basis of local-by-global novelty interactions. Positive interaction was defined as a greater response to the double surprise LDGD condition compared to LSGD. Negative interaction was defined as a weaker response to LDGD. Positive interaction was more frequent than negative interaction and was primarily found in auditory cortex. Negative interaction typically occurred in prefrontal cortex and was more sensitive to general anesthesia. Temporo-parietal auditory-related areas exhibited both types of interaction. These interactions may have relevance in a clinical setting as biomarkers of conscious perception in the assessment of depth of anesthesia and disorders of consciousness. |
| first_indexed | 2024-12-14T17:27:54Z |
| format | Article |
| id | doaj.art-31e0348be9f341b081645e824455a8af |
| institution | Directory Open Access Journal |
| issn | 1662-5161 |
| language | English |
| last_indexed | 2024-12-14T17:27:54Z |
| publishDate | 2021-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Human Neuroscience |
| spelling | doaj.art-31e0348be9f341b081645e824455a8af2022-12-21T22:53:10ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612021-10-011510.3389/fnhum.2021.737230737230Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human SubjectsKirill V. Nourski0Kirill V. Nourski1Mitchell Steinschneider2Mitchell Steinschneider3Ariane E. Rhone4Rashmi N. Mueller5Rashmi N. Mueller6Hiroto Kawasaki7Matthew I. Banks8Matthew I. Banks9Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesIowa Neuroscience Institute, The University of Iowa, Iowa City, IA, United StatesDepartment of Neurology, Albert Einstein College of Medicine, Bronx, NY, United StatesDepartment of Neuroscience, Albert Einstein College of Medicine, Bronx, NY, United StatesHuman Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesHuman Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesDepartment of Anesthesia, The University of Iowa, Iowa City, IA, United StatesHuman Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesDepartment of Anesthesiology, University of Wisconsin School of Medicine and Public Health, Madison, WI, United StatesDepartment of Neuroscience, University of Wisconsin School of Medicine and Public Health, Madison, WI, United StatesIn everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activity associated with predictable backgrounds and emphasizes detection of changes in the environment. In real life, the brain must resolve multiple unexpected sensory events occurring over different time scales. The local/global deviant experimental paradigm examines auditory predictive coding over multiple time scales. For short-term novelty [hundreds of milliseconds; local deviance (LD)], sequences of identical sounds (/xxxxx/) are interspersed with sequences that contain deviants (/xxxxy/). Long-term novelty [several seconds; global deviance (GD)] is created using either (a) frequent /xxxxx/ and infrequent /xxxxy/ sequences, or (b) frequent /xxxxy/ and infrequent /xxxxx/ sequences. In scenario (a), there is both an LD and a GD effect (LDGD, “double surprise”). In (b), the global deviant is a local standard, i.e., sequence of identical sounds (LSGD). Cortical responses reflecting LD and GD originate in different brain areas, have a different time course, and are differentially sensitive to general anesthesia. Neural processes underlying LD and GD have been shown to interact, reflecting overlapping networks subserving the detection of novel auditory stimuli. This study examined these interactions using intracranial electroencephalography in neurosurgical patients. Subjects performed a GD target detection task before and during induction of anesthesia with propofol. Recordings were made from the auditory cortex, surrounding auditory-related and prefrontal cortex in awake, sedated, and unresponsive states. High gamma activity was used to measure the neural basis of local-by-global novelty interactions. Positive interaction was defined as a greater response to the double surprise LDGD condition compared to LSGD. Negative interaction was defined as a weaker response to LDGD. Positive interaction was more frequent than negative interaction and was primarily found in auditory cortex. Negative interaction typically occurred in prefrontal cortex and was more sensitive to general anesthesia. Temporo-parietal auditory-related areas exhibited both types of interaction. These interactions may have relevance in a clinical setting as biomarkers of conscious perception in the assessment of depth of anesthesia and disorders of consciousness.https://www.frontiersin.org/articles/10.3389/fnhum.2021.737230/fullauditory cortexconsciousnessgeneral anesthesiahigh gammaiEEGlocal/global deviant |
| spellingShingle | Kirill V. Nourski Kirill V. Nourski Mitchell Steinschneider Mitchell Steinschneider Ariane E. Rhone Rashmi N. Mueller Rashmi N. Mueller Hiroto Kawasaki Matthew I. Banks Matthew I. Banks Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects Frontiers in Human Neuroscience auditory cortex consciousness general anesthesia high gamma iEEG local/global deviant |
| title | Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects |
| title_full | Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects |
| title_fullStr | Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects |
| title_full_unstemmed | Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects |
| title_short | Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects |
| title_sort | arousal state dependence of interactions between short and long term auditory novelty responses in human subjects |
| topic | auditory cortex consciousness general anesthesia high gamma iEEG local/global deviant |
| url | https://www.frontiersin.org/articles/10.3389/fnhum.2021.737230/full |
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