Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1
Standard models for spatial and episodic memory suggest that the lateral entorhinal cortex (LEC) and medial entorhinal cortex (MEC) send parallel independent inputs to the hippocampus, each carrying different types of information. Here, we evaluate the possibility that information is integrated betw...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-12-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/83008 |
| _version_ | 1797959957452161024 |
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| author | Brianna Vandrey Jack Armstrong Christina M Brown Derek LF Garden Matthew F Nolan |
| author_facet | Brianna Vandrey Jack Armstrong Christina M Brown Derek LF Garden Matthew F Nolan |
| author_sort | Brianna Vandrey |
| collection | DOAJ |
| description | Standard models for spatial and episodic memory suggest that the lateral entorhinal cortex (LEC) and medial entorhinal cortex (MEC) send parallel independent inputs to the hippocampus, each carrying different types of information. Here, we evaluate the possibility that information is integrated between divisions of the entorhinal cortex prior to reaching the hippocampus. We demonstrate that, in mice, fan cells in layer 2 (L2) of LEC that receive neocortical inputs, and that project to the hippocampal dentate gyrus, also send axon collaterals to layer 1 (L1) of the MEC. Activation of inputs from fan cells evokes monosynaptic glutamatergic excitation of stellate and pyramidal cells in L2 of the MEC, typically followed by inhibition that contains fast and slow components mediated by GABAA and GABAB receptors, respectively. Inputs from fan cells also directly activate interneurons in L1 and L2 of MEC, with synaptic connections from L1 interneurons accounting for slow feedforward inhibition of L2 principal cell populations. The relative strength of excitation and inhibition following fan cell activation differs substantially between neurons and is largely independent of anatomical location. Our results demonstrate that the LEC, in addition to directly influencing the hippocampus, can activate or inhibit major hippocampal inputs arising from the MEC. Thus, local circuits in the superficial MEC may combine spatial information with sensory and higher order signals from the LEC, providing a substrate for integration of ‘what’ and ‘where’ components of episodic memories. |
| first_indexed | 2024-04-11T00:39:00Z |
| format | Article |
| id | doaj.art-48f89fb98f6d4d27ab12da392ddd621f |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T00:39:00Z |
| publishDate | 2022-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-48f89fb98f6d4d27ab12da392ddd621f2023-01-06T09:38:22ZengeLife Sciences Publications LtdeLife2050-084X2022-12-011110.7554/eLife.83008Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1Brianna Vandrey0Jack Armstrong1Christina M Brown2Derek LF Garden3https://orcid.org/0000-0003-3336-3791Matthew F Nolan4https://orcid.org/0000-0003-1062-6501Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United KingdomCentre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United KingdomCentre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United KingdomCentre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United KingdomCentre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom; Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, United Kingdom; Centre for Statistics, University of Edinburgh, Edinburgh, United KingdomStandard models for spatial and episodic memory suggest that the lateral entorhinal cortex (LEC) and medial entorhinal cortex (MEC) send parallel independent inputs to the hippocampus, each carrying different types of information. Here, we evaluate the possibility that information is integrated between divisions of the entorhinal cortex prior to reaching the hippocampus. We demonstrate that, in mice, fan cells in layer 2 (L2) of LEC that receive neocortical inputs, and that project to the hippocampal dentate gyrus, also send axon collaterals to layer 1 (L1) of the MEC. Activation of inputs from fan cells evokes monosynaptic glutamatergic excitation of stellate and pyramidal cells in L2 of the MEC, typically followed by inhibition that contains fast and slow components mediated by GABAA and GABAB receptors, respectively. Inputs from fan cells also directly activate interneurons in L1 and L2 of MEC, with synaptic connections from L1 interneurons accounting for slow feedforward inhibition of L2 principal cell populations. The relative strength of excitation and inhibition following fan cell activation differs substantially between neurons and is largely independent of anatomical location. Our results demonstrate that the LEC, in addition to directly influencing the hippocampus, can activate or inhibit major hippocampal inputs arising from the MEC. Thus, local circuits in the superficial MEC may combine spatial information with sensory and higher order signals from the LEC, providing a substrate for integration of ‘what’ and ‘where’ components of episodic memories.https://elifesciences.org/articles/83008memoryneural circuithippocampal formationoptogenetics |
| spellingShingle | Brianna Vandrey Jack Armstrong Christina M Brown Derek LF Garden Matthew F Nolan Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 eLife memory neural circuit hippocampal formation optogenetics |
| title | Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 |
| title_full | Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 |
| title_fullStr | Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 |
| title_full_unstemmed | Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 |
| title_short | Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 |
| title_sort | fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1 |
| topic | memory neural circuit hippocampal formation optogenetics |
| url | https://elifesciences.org/articles/83008 |
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