Transversal functional connectivity and scene-specific processing in the human entorhinal-hippocampal circuitry
- German Center for Neurodegenerative Diseases, Germany
- Leibniz Institute for Neurobiology, Germany
- Otto-von-Guericke University Magdeburg, Germany
Abstract
Scene and object information reach the entorhinal-hippocampal circuitry in partly segregated cortical processing streams. Converging evidence suggests that such information-specific streams organize the cortical - entorhinal interaction and the circuitry's inner communication along the transversal axis of hippocampal subiculum and CA1. Here, we leveraged ultra-high field functional imaging and advance Maass, Berron et al. (2015) who report two functional routes segregating the entorhinal cortex (EC) and the subiculum. We identify entorhinal subregions based on preferential functional connectivity with perirhinal Area 35 and 36, parahippocampal and retrosplenial cortical sources (referred to as ECArea35-based, ECArea36-based, ECPHC-based, ECRSC-based, respectively). Our data show specific scene processing in the functionally connected ECPHC-based and distal subiculum. Another route, that functionally connects the ECArea35-based and a newly identified ECRSC-based with the subiculum/CA1 border, however, shows no selectivity between object and scene conditions. Our results are consistent with transversal information-specific pathways in the human entorhinal-hippocampal circuitry, with anatomically organized convergence of cortical processing streams and a unique route for scene information. Our study thus further characterizes the functional organization of this circuitry and its information-specific role in memory function.
Data availability
Source data that contain numerical data used to generate Figure 2, Figure 3, Figure 4, Appendix 1 Figure 2, Appendix 1 Figure 3, Appendix 1 Figure 4, Appendix 5 Figure 1 as well as group-level statistical maps (referred to as Source Code 1-16) that underlie Figure 1, Figure 2, Appendix 1 Figure 1, Appendix 1 Figure 2, Appendix 3 Figure 1, Appendix 3 Figure 2 and Appendix 4 Figure 1 have been provided under:Open Science Framework. ID 9v3qp. https://osf.io/9v3qp
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Source Data from Functional Connectivity and Information Processing in the Entorhinal-Hippocampal CircuitryOpen Science Framework. ID 9v3qp.
Article and author information
Author details
Magdalena M Sauvage
Funding
Horizon 2020 Research and Innovation Programme (785907 (HBP SGA2) and 945539 (HBP SGA3))
- Emrah Düzel
Deutsche Forschungsgemeinschaft (Project-ID 42589994)
- Magdalena M Sauvage
- Emrah Düzel
HORIZON EUROPE Marie Sklodowska-Curie Actions (843074)
- David Berron
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Informed consent and consent to publish was obtained from human participants.The study received approval by the ethics committee of Otto-von-Guericke University, Magdeburg (Germany) under reference number 128/14.
Copyright
© 2022, Grande et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Transversal functional connectivity and scene-specific processing in the human entorhinal-hippocampal circuitry
eLife 11:e76479.
https://doi.org/10.7554/eLife.76479
Further reading
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- Neuroscience
To encode continuous sound stimuli, the inner hair cell (IHC) ribbon synapses utilize calcium-binding proteins (CaBPs), which reduce the inactivation of their CaV1.3 calcium channels. Mutations in the CABP2 gene underlie non-syndromic autosomal recessive hearing loss DFNB93. Besides CaBP2, the structurally related CaBP1 is highly abundant in the IHCs. Here, we investigated how the two CaBPs cooperatively regulate IHC synaptic function. In Cabp1/2 double-knockout mice, we find strongly enhanced CaV1.3 inactivation, slowed recovery from inactivation and impaired sustained exocytosis. Already mild IHC activation further reduces the availability of channels to trigger synaptic transmission and may effectively silence synapses. Spontaneous and sound-evoked responses of spiral ganglion neurons in vivo are strikingly reduced and strongly depend on stimulation rates. Transgenic expression of CaBP2 leads to substantial recovery of IHC synaptic function and hearing sensitivity. We conclude that CaBP1 and 2 act together to suppress voltage- and calcium-dependent inactivation of IHC CaV1.3 channels in order to support sufficient rate of exocytosis and enable fast, temporally precise and indefatigable sound encoding.
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- Neuroscience
Neural diversity can expand the encoding capacity of a circuitry. A striking example of diverse structure and function is presented by the afferent synapses between inner hair cells (IHCs) and spiral ganglion neurons (SGNs) in the cochlea. Presynaptic active zones at the pillar IHC side activate at lower IHC potentials than those of the modiolar side that have more presynaptic Ca2+ channels. The postsynaptic SGNs differ in their spontaneous firing rates, sound thresholds, and operating ranges. While a causal relationship between synaptic heterogeneity and neural response diversity seems likely, experimental evidence linking synaptic and SGN physiology has remained difficult to obtain. Here, we aimed at bridging this gap by ex vivo paired recordings of murine IHCs and postsynaptic SGN boutons with stimuli and conditions aimed to mimic those of in vivo SGN characterization. Synapses with high spontaneous rate of release (SR) were found predominantly on the pillar side of the IHC. These high SR synapses had larger and more temporally compact spontaneous EPSCs, lower voltage thresholds, tighter coupling of Ca2+ channels and vesicular release sites, shorter response latencies, and higher initial release rates. This study indicates that synaptic heterogeneity in IHCs directly contributes to the diversity of spontaneous and sound-evoked firing of SGNs.
