Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices
Multisensory integration in primary auditory (A1), visual (V1), and somatosensory cortex (S1) is substantially mediated by their direct interconnections and by thalamic inputs across the sensory modalities. We have previously shown in rodents (Mongolian gerbils) that during postnatal development, th...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-09-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fncir.2019.00061/full |
| _version_ | 1818967064040177664 |
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| author | Tamar Macharadze Tamar Macharadze Eike Budinger Eike Budinger Michael Brosch Michael Brosch Henning Scheich Henning Scheich Frank W. Ohl Frank W. Ohl Frank W. Ohl Julia U. Henschke |
| author_facet | Tamar Macharadze Tamar Macharadze Eike Budinger Eike Budinger Michael Brosch Michael Brosch Henning Scheich Henning Scheich Frank W. Ohl Frank W. Ohl Frank W. Ohl Julia U. Henschke |
| author_sort | Tamar Macharadze |
| collection | DOAJ |
| description | Multisensory integration in primary auditory (A1), visual (V1), and somatosensory cortex (S1) is substantially mediated by their direct interconnections and by thalamic inputs across the sensory modalities. We have previously shown in rodents (Mongolian gerbils) that during postnatal development, the anatomical and functional strengths of these crossmodal and also of sensory matched connections are determined by early auditory, somatosensory, and visual experience. Because supragranular layer III pyramidal neurons are major targets of corticocortical and thalamocortical connections, we investigated in this follow-up study how the loss of early sensory experience changes their dendritic morphology. Gerbils were sensory deprived early in development by either bilateral sciatic nerve transection at postnatal day (P) 5, ototoxic inner hair cell damage at P10, or eye enucleation at P10. Sholl and branch order analyses of Golgi-stained layer III pyramidal neurons at P28, which demarcates the end of the sensory critical period in this species, revealed that visual and somatosensory deprivation leads to a general increase of apical and basal dendritic branching in A1, V1, and S1. In contrast, dendritic branching, particularly of apical dendrites, decreased in all three areas following auditory deprivation. Generally, the number of spines, and consequently spine density, along the apical and basal dendrites decreased in both sensory deprived and non-deprived cortical areas. Therefore, we conclude that the loss of early sensory experience induces a refinement of corticocortical crossmodal and other cortical and thalamic connections by pruning of dendritic spines at the end of the critical period. Based on present and previous own results and on findings from the literature, we propose a scenario for multisensory development following early sensory loss. |
| first_indexed | 2024-12-20T13:42:51Z |
| format | Article |
| id | doaj.art-d4fda8d9b5f64666a3ec424e90449e34 |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-12-20T13:42:51Z |
| publishDate | 2019-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-d4fda8d9b5f64666a3ec424e90449e342022-12-21T19:38:46ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102019-09-011310.3389/fncir.2019.00061479984Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory CorticesTamar Macharadze0Tamar Macharadze1Eike Budinger2Eike Budinger3Michael Brosch4Michael Brosch5Henning Scheich6Henning Scheich7Frank W. Ohl8Frank W. Ohl9Frank W. Ohl10Julia U. Henschke11Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg, GermanyClinic for Anesthesiology and Intensive Care Medicine, Otto von Guericke University Hospital, Magdeburg, GermanyDepartment Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg, GermanyCenter for Behavioral Brain Sciences, Magdeburg, GermanyCenter for Behavioral Brain Sciences, Magdeburg, GermanySpecial Lab Primate Neurobiology, Leibniz Institute for Neurobiology, Magdeburg, GermanyCenter for Behavioral Brain Sciences, Magdeburg, GermanyEmeritus Group Lifelong Learning, Leibniz Institute for Neurobiology, Magdeburg, GermanyDepartment Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg, GermanyCenter for Behavioral Brain Sciences, Magdeburg, GermanyInstitute for Biology, Otto von Guericke University, Magdeburg, GermanyInstitute of Cognitive Neurology and Dementia Research (IKND), Otto von Guericke University, Magdeburg, GermanyMultisensory integration in primary auditory (A1), visual (V1), and somatosensory cortex (S1) is substantially mediated by their direct interconnections and by thalamic inputs across the sensory modalities. We have previously shown in rodents (Mongolian gerbils) that during postnatal development, the anatomical and functional strengths of these crossmodal and also of sensory matched connections are determined by early auditory, somatosensory, and visual experience. Because supragranular layer III pyramidal neurons are major targets of corticocortical and thalamocortical connections, we investigated in this follow-up study how the loss of early sensory experience changes their dendritic morphology. Gerbils were sensory deprived early in development by either bilateral sciatic nerve transection at postnatal day (P) 5, ototoxic inner hair cell damage at P10, or eye enucleation at P10. Sholl and branch order analyses of Golgi-stained layer III pyramidal neurons at P28, which demarcates the end of the sensory critical period in this species, revealed that visual and somatosensory deprivation leads to a general increase of apical and basal dendritic branching in A1, V1, and S1. In contrast, dendritic branching, particularly of apical dendrites, decreased in all three areas following auditory deprivation. Generally, the number of spines, and consequently spine density, along the apical and basal dendrites decreased in both sensory deprived and non-deprived cortical areas. Therefore, we conclude that the loss of early sensory experience induces a refinement of corticocortical crossmodal and other cortical and thalamic connections by pruning of dendritic spines at the end of the critical period. Based on present and previous own results and on findings from the literature, we propose a scenario for multisensory development following early sensory loss.https://www.frontiersin.org/article/10.3389/fncir.2019.00061/fullcortexcrossmodaldeprivationdevelopmentGolgiintegration |
| spellingShingle | Tamar Macharadze Tamar Macharadze Eike Budinger Eike Budinger Michael Brosch Michael Brosch Henning Scheich Henning Scheich Frank W. Ohl Frank W. Ohl Frank W. Ohl Julia U. Henschke Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices Frontiers in Neural Circuits cortex crossmodal deprivation development Golgi integration |
| title | Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices |
| title_full | Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices |
| title_fullStr | Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices |
| title_full_unstemmed | Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices |
| title_short | Early Sensory Loss Alters the Dendritic Branching and Spine Density of Supragranular Pyramidal Neurons in Rodent Primary Sensory Cortices |
| title_sort | early sensory loss alters the dendritic branching and spine density of supragranular pyramidal neurons in rodent primary sensory cortices |
| topic | cortex crossmodal deprivation development Golgi integration |
| url | https://www.frontiersin.org/article/10.3389/fncir.2019.00061/full |
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