Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex.
Earlier studies demonstrate that when the frequency of rhythmic tone sequences or streams is task relevant, ongoing excitability fluctuations (oscillations) of neuronal ensembles in primary auditory cortex (A1) entrain to stimulation in a frequency dependent way that sharpens frequency tuning. The p...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2015-12-01
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| Series: | Frontiers in Human Neuroscience |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fnhum.2015.00655/full |
| _version_ | 1811327515858305024 |
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| author | Monica Noelle O'Connell Annamaria eBarczak Deborah eRoss Tammy eMcGinnis Charles E Schroeder Charles E Schroeder Peter eLakatos Peter eLakatos |
| author_facet | Monica Noelle O'Connell Annamaria eBarczak Deborah eRoss Tammy eMcGinnis Charles E Schroeder Charles E Schroeder Peter eLakatos Peter eLakatos |
| author_sort | Monica Noelle O'Connell |
| collection | DOAJ |
| description | Earlier studies demonstrate that when the frequency of rhythmic tone sequences or streams is task relevant, ongoing excitability fluctuations (oscillations) of neuronal ensembles in primary auditory cortex (A1) entrain to stimulation in a frequency dependent way that sharpens frequency tuning. The phase distribution across A1 neuronal ensembles at time points when attended stimuli are predicted to occur reflects the focus of attention along the spectral attribute of auditory stimuli. This study examined how neuronal activity is modulated if only the temporal features of rhythmic stimulus streams are relevant. We presented macaques with auditory clicks arranged in 33 Hz (gamma timescale) quintets, repeated at a 1.6 Hz (delta timescale) rate. Such multi-scale, hierarchically organized temporal structure is characteristic of vocalizations and other natural stimuli. Monkeys were required to detect and respond to deviations in the temporal pattern of gamma quintets. As expected, engagement in the auditory task resulted in the multi-scale entrainment of delta- and gamma-band neuronal oscillations across all of A1. Surprisingly, however, the phase-alignment, and thus, the physiological impact of entrainment differed across the tonotopic map in A1. In the region of 11-16 kHz representation, entrainment most often aligned high excitability oscillatory phases with task-relevant events in the input stream and thus resulted in response enhancement. In the remainder of the A1 sites, entrainment generally resulted in response suppression. Our data indicate that the suppressive effects were due to low excitability phase delta oscillatory entrainment and the phase amplitude coupling of delta and gamma oscillations. Regardless of the phase or frequency, entrainment appeared stronger in left A1, indicative of the hemispheric lateralization of auditory function. |
| first_indexed | 2024-04-13T15:08:11Z |
| format | Article |
| id | doaj.art-b58b5e3f0b4a4ebd999422c6b44941d7 |
| institution | Directory Open Access Journal |
| issn | 1662-5161 |
| language | English |
| last_indexed | 2024-04-13T15:08:11Z |
| publishDate | 2015-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Human Neuroscience |
| spelling | doaj.art-b58b5e3f0b4a4ebd999422c6b44941d72022-12-22T02:42:06ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612015-12-01910.3389/fnhum.2015.00655165995Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex.Monica Noelle O'Connell0Annamaria eBarczak1Deborah eRoss2Tammy eMcGinnis3Charles E Schroeder4Charles E Schroeder5Peter eLakatos6Peter eLakatos7Nathan Kline InstituteNathan Kline InstituteNathan Kline InstituteNathan Kline InstituteNathan Kline InstituteColumbia College of Physicians and SurgeonsNathan Kline InstituteNYU School of MedicineEarlier studies demonstrate that when the frequency of rhythmic tone sequences or streams is task relevant, ongoing excitability fluctuations (oscillations) of neuronal ensembles in primary auditory cortex (A1) entrain to stimulation in a frequency dependent way that sharpens frequency tuning. The phase distribution across A1 neuronal ensembles at time points when attended stimuli are predicted to occur reflects the focus of attention along the spectral attribute of auditory stimuli. This study examined how neuronal activity is modulated if only the temporal features of rhythmic stimulus streams are relevant. We presented macaques with auditory clicks arranged in 33 Hz (gamma timescale) quintets, repeated at a 1.6 Hz (delta timescale) rate. Such multi-scale, hierarchically organized temporal structure is characteristic of vocalizations and other natural stimuli. Monkeys were required to detect and respond to deviations in the temporal pattern of gamma quintets. As expected, engagement in the auditory task resulted in the multi-scale entrainment of delta- and gamma-band neuronal oscillations across all of A1. Surprisingly, however, the phase-alignment, and thus, the physiological impact of entrainment differed across the tonotopic map in A1. In the region of 11-16 kHz representation, entrainment most often aligned high excitability oscillatory phases with task-relevant events in the input stream and thus resulted in response enhancement. In the remainder of the A1 sites, entrainment generally resulted in response suppression. Our data indicate that the suppressive effects were due to low excitability phase delta oscillatory entrainment and the phase amplitude coupling of delta and gamma oscillations. Regardless of the phase or frequency, entrainment appeared stronger in left A1, indicative of the hemispheric lateralization of auditory function.http://journal.frontiersin.org/Journal/10.3389/fnhum.2015.00655/fullMacaca mulattaneuronal oscillationsprimary auditory cortexentrainmentintracorticaltonotopic map |
| spellingShingle | Monica Noelle O'Connell Annamaria eBarczak Deborah eRoss Tammy eMcGinnis Charles E Schroeder Charles E Schroeder Peter eLakatos Peter eLakatos Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. Frontiers in Human Neuroscience Macaca mulatta neuronal oscillations primary auditory cortex entrainment intracortical tonotopic map |
| title | Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. |
| title_full | Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. |
| title_fullStr | Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. |
| title_full_unstemmed | Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. |
| title_short | Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. |
| title_sort | multi scale entrainment of coupled neuronal oscillations in primary auditory cortex |
| topic | Macaca mulatta neuronal oscillations primary auditory cortex entrainment intracortical tonotopic map |
| url | http://journal.frontiersin.org/Journal/10.3389/fnhum.2015.00655/full |
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