Synthesis of a comprehensive population code for contextual features in the awake sensory cortex
How cortical circuits build representations of complex objects is poorly understood. Individual neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific global stimulus features. Groups of neurons identifying different global features must then assemble into a po...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-11-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/62687 |
| _version_ | 1828166860883886080 |
|---|---|
| author | Evan H Lyall Daniel P Mossing Scott R Pluta Yun Wen Chu Amir Dudai Hillel Adesnik |
| author_facet | Evan H Lyall Daniel P Mossing Scott R Pluta Yun Wen Chu Amir Dudai Hillel Adesnik |
| author_sort | Evan H Lyall |
| collection | DOAJ |
| description | How cortical circuits build representations of complex objects is poorly understood. Individual neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific global stimulus features. Groups of neurons identifying different global features must then assemble into a population that forms a comprehensive code for these global stimulus properties. Although the logic for how single neurons summate over their spatial inputs has been well explored in anesthetized animals, how large groups of neurons compose a flexible population code of higher-order features in awake animals is not known. To address this question, we probed the integration and population coding of higher-order stimuli in the somatosensory and visual cortices of awake mice using two-photon calcium imaging across cortical layers. We developed a novel tactile stimulator that allowed the precise measurement of spatial summation even in actively whisking mice. Using this system, we found a sparse but comprehensive population code for higher-order tactile features that depends on a heterogeneous and neuron-specific logic of spatial summation beyond the receptive field. Different somatosensory cortical neurons summed specific combinations of sensory inputs supra-linearly, but integrated other inputs sub-linearly, leading to selective responses to higher-order features. Visual cortical populations employed a nearly identical scheme to generate a comprehensive population code for contextual stimuli. These results suggest that a heterogeneous logic of input-specific supra-linear summation may represent a widespread cortical mechanism for the synthesis of sparse higher-order feature codes in neural populations. This may explain how the brain exploits the thalamocortical expansion of dimensionality to encode arbitrary complex features of sensory stimuli. |
| first_indexed | 2024-04-12T02:09:27Z |
| format | Article |
| id | doaj.art-c3d23e86754244249d4048fba5a410e3 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:09:27Z |
| publishDate | 2021-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-c3d23e86754244249d4048fba5a410e32022-12-22T03:52:27ZengeLife Sciences Publications LtdeLife2050-084X2021-11-011010.7554/eLife.62687Synthesis of a comprehensive population code for contextual features in the awake sensory cortexEvan H Lyall0https://orcid.org/0000-0002-6946-7333Daniel P Mossing1https://orcid.org/0000-0002-9939-4788Scott R Pluta2https://orcid.org/0000-0002-3057-8095Yun Wen Chu3Amir Dudai4Hillel Adesnik5https://orcid.org/0000-0002-3796-8643Biophysics Graduate Group, Berkeley, United States; Department of Molecular and Cell Biology, Berkeley, United StatesBiophysics Graduate Group, Berkeley, United States; Department of Molecular and Cell Biology, Berkeley, United StatesDepartment of Molecular and Cell Biology, Berkeley, United StatesDepartment of Molecular and Cell Biology, Berkeley, United StatesThe Edmond and Lily Safra Center for Brain Sciences and The Life Sciences Institute, The Hebrew University of Jerusalem, Jerusalem, IsraelDepartment of Molecular and Cell Biology, Berkeley, United States; The Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United StatesHow cortical circuits build representations of complex objects is poorly understood. Individual neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific global stimulus features. Groups of neurons identifying different global features must then assemble into a population that forms a comprehensive code for these global stimulus properties. Although the logic for how single neurons summate over their spatial inputs has been well explored in anesthetized animals, how large groups of neurons compose a flexible population code of higher-order features in awake animals is not known. To address this question, we probed the integration and population coding of higher-order stimuli in the somatosensory and visual cortices of awake mice using two-photon calcium imaging across cortical layers. We developed a novel tactile stimulator that allowed the precise measurement of spatial summation even in actively whisking mice. Using this system, we found a sparse but comprehensive population code for higher-order tactile features that depends on a heterogeneous and neuron-specific logic of spatial summation beyond the receptive field. Different somatosensory cortical neurons summed specific combinations of sensory inputs supra-linearly, but integrated other inputs sub-linearly, leading to selective responses to higher-order features. Visual cortical populations employed a nearly identical scheme to generate a comprehensive population code for contextual stimuli. These results suggest that a heterogeneous logic of input-specific supra-linear summation may represent a widespread cortical mechanism for the synthesis of sparse higher-order feature codes in neural populations. This may explain how the brain exploits the thalamocortical expansion of dimensionality to encode arbitrary complex features of sensory stimuli.https://elifesciences.org/articles/62687visual cortexbarrel cortexsparse codesreceptive fieldtwo photon calcium imagingneural coding |
| spellingShingle | Evan H Lyall Daniel P Mossing Scott R Pluta Yun Wen Chu Amir Dudai Hillel Adesnik Synthesis of a comprehensive population code for contextual features in the awake sensory cortex eLife visual cortex barrel cortex sparse codes receptive field two photon calcium imaging neural coding |
| title | Synthesis of a comprehensive population code for contextual features in the awake sensory cortex |
| title_full | Synthesis of a comprehensive population code for contextual features in the awake sensory cortex |
| title_fullStr | Synthesis of a comprehensive population code for contextual features in the awake sensory cortex |
| title_full_unstemmed | Synthesis of a comprehensive population code for contextual features in the awake sensory cortex |
| title_short | Synthesis of a comprehensive population code for contextual features in the awake sensory cortex |
| title_sort | synthesis of a comprehensive population code for contextual features in the awake sensory cortex |
| topic | visual cortex barrel cortex sparse codes receptive field two photon calcium imaging neural coding |
| url | https://elifesciences.org/articles/62687 |
| work_keys_str_mv | AT evanhlyall synthesisofacomprehensivepopulationcodeforcontextualfeaturesintheawakesensorycortex AT danielpmossing synthesisofacomprehensivepopulationcodeforcontextualfeaturesintheawakesensorycortex AT scottrpluta synthesisofacomprehensivepopulationcodeforcontextualfeaturesintheawakesensorycortex AT yunwenchu synthesisofacomprehensivepopulationcodeforcontextualfeaturesintheawakesensorycortex AT amirdudai synthesisofacomprehensivepopulationcodeforcontextualfeaturesintheawakesensorycortex AT hilleladesnik synthesisofacomprehensivepopulationcodeforcontextualfeaturesintheawakesensorycortex |