Novel encoding and updating of positional, or directional, spatial cues are processed by distinct hippocampal subfields: evidence for parallel information processing and the "what" stream
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The specific roles of hippocampal subfields in spatial information processing and encoding are, as yet, unclear. The parallel map theory postulates that whereas the CA1 processes discrete environmental features (positional cues used to generate a "sketch map"), the dentate gyrus (DG) processes large navigation-relevant landmarks (directional cues used to generate a "bearing map"). Additionally, the two-streams hypothesis suggests that hippocampal subfields engage in differentiated processing of information from the "where" and the "what" streams. We investigated these hypotheses by analyzing the effect of exploration of discrete "positional" features and large "directional" spatial landmarks on hippocampal neuronal activity in rats. As an indicator of neuronal activity we measured the mRNA induction of the immediate early genes (IEGs), Arc and Homer1a. We observed an increase of this IEG mRNA in CA1 neurons of the distal neuronal compartment and in proximal CA3, after novel spatial exploration of discrete positional cues, whereas novel exploration of directional cues led to increases in IEG mRNA in the lower blade of the DG and in proximal CA3. Strikingly, the CA1 did not respond to directional cues and the DG did not respond to positional cues. Our data provide evidence for both the parallel map theory and the two-streams hypothesis and suggest a precise compartmentalization of the encoding and processing of "what" and "where" information occurs within the hippocampal subfields.
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In a setting of exploring three small "positionally" distinct objects, the distal CA1 and proximal CA3 were recruited during the recognition of a novel object, whereas the proximal CA3 and lower blade of dentate gyrus, but not CA1, were involved in novel object recognition during exploring three large "directionally" distinct objects.
“For instance, in a setting of exploring three small “positionally” distinct objects, the distal CA1 and proximal CA3, which preferentially receive “what” information (Mishkin et al., 1983), were recruited during the recognition of a novel object (increased mRNA of the immediate early genes Arc and Homer1a), whereas the proximal CA3 and lower blade of dentate gyrus, but not CA1, were involved in”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Hoang et al., 2018
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Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Object vision and spatial vision: Two cortical pathways
Mishkin, M., Ungerleider, L. G., & Macko, K. A. (1983) · Trends in Neurosciences · doi:10.1016/0166-2236(83)90190-x · Cited by 2,947 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Spatial representation in the entorhinal cortex
Fyhn, M., Molden, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2004) · Science · doi:10.1126/science.1099901 · Cited by 1,339 · see citing works
Lyford, G. L., Yamagata, K., Kaufmann, W. E., Barnes, C. A., Sanders, L. K., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Lanahan, A. A., & Worley, P. F. (1995) · Neuron · doi:10.1016/0896-6273(95)90299-6 · Cited by 1,212 · see citing works
Homer: a protein that selectively binds metabotropic glutamate receptors
Brakeman, P., Lanahan, A. A., O’Brien, R., Roche, K. W., Barnes, C. A., Huganir, R. L., & Worley, P. F. (1997) · Nature · doi:10.1038/386284a0 · Cited by 1,115 · see citing works
Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles
Guzowski, J. F., McNaughton, B. L., Barnes, C. A., & Worley, P. F. (1999) · Nature Neuroscience · doi:10.1038/16046 · Cited by 1,035 · see citing works
Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat
Ishizuka, N., Weber, J., & Amaral, D. G. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950407 · Cited by 899 · see citing works
Somatodendritic expression of an immediate early gene is regulated by synaptic activity.
Link, W., Konietzko, U., Kauselmann, G., Krug, M., Schwanke, B., Frey, U., & Kuhl, D. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5734 · Cited by 706 · see citing works
Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus
Hargreaves, E. L., Rao, G., Lee, I., & Knierim, J. J. (2005) · Science · doi:10.1126/science.1110449 · Cited by 685 · see citing works
Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains.
Adams, J. C. (1992) · Journal of Histochemistry & Cytochemistry · doi:10.1177/40.10.1527370 · Cited by 644 · see citing works
Anatomical organization of the parahippocampal-hippocampal network
WITTER, M. P., WOUTERLOOD, F. G., NABER, P. A., & VAN HAEFTEN, T. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06716.x · Cited by 567 · see citing works
The Immediate Early Gene Arc / Arg3.1 : Regulation, Mechanisms, and Function
Bramham, C. R., Worley, P. F., Moore, M. J., & Guzowski, J. F. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3864-08.2008 · Cited by 480 · see citing works
Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex
Deshmukh, S. S., & Knierim, J. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00069 · Cited by 454 · see citing works
Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas
Kerr, K. M., Agster, K. L., Furtak, S. C., & Burwell, R. D. (2007) · Hippocampus · doi:10.1002/hipo.20315 · Cited by 433 · see citing works
Mapping behaviorally relevant neural circuits with immediate-early gene expression
Guzowski, J. F., Timlin, J. A., Roysam, B., McNaughton, B. L., Worley, P. F., & Barnes, C. A. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.08.018 · Cited by 404 · see citing works
Arc in synaptic plasticity: from gene to behavior
Korb, E., & Finkbeiner, S. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.007 · Cited by 388 · see citing works
Chawla, M. K., Guzowski, J. F., Ramı́rez-Amaya, V., Lipa, P., Hoffman, K. L., Marriott, L. K., Worley, P. F., McNaughton, B. L., & Barnes, C. A. (2005) · Hippocampus · doi:10.1002/hipo.20091 · Cited by 375 · see citing works
Memory Representation within the Parahippocampal Region
Young, B. J., Otto, T., Fox, G. D., & Eichenbaum, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05183.1997 · Cited by 363 · see citing works
Novelty acquisition is associated with induction of hippocampal long-term depression
Manahan‐Vaughan, D., & Braunewell, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.15.8739 · Cited by 358 · see citing works
Self-citationKemp, A., & Manahan‐Vaughan, D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402650101 · Cited by 356 · see citing works
Self-citationHippocampal long-term depression: master or minion in declarative memory processes?
Kemp, A., & Manahan-Vaughan, D. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.01.002 · Cited by 336 · see citing works
Self-citationUnpacking the cognitive map: The parallel map theory of hippocampal function.
Jacobs, L. F., & Schenk, F. (2003) · Psychological Review · doi:10.1037/0033-295x.110.2.285 · Cited by 325 · see citing works
An autoradiographic study of the efferent connections of the entorhinal cortex in the rat
Wyss, J. M. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901990405 · Cited by 312 · see citing works
Vazdarjanova, A. I., McNaughton, B. L., Barnes, C. A., Worley, P. F., & Guzowski, J. F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-23-10067.2002 · Cited by 307 · see citing works
Furtak, S. C., Wei, S., Agster, K. L., & Burwell, R. D. (2007) · Hippocampus · doi:10.1002/hipo.20314 · Cited by 282 · see citing works
Spatial Representation along the Proximodistal Axis of CA1
Henriksen, E. J., Colgin, L. L., Barnes, C. A., Witter, M. P., Moser, M., & Moser, E. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.042 · Cited by 260 · see citing works
Intrinsic and extrinsic wiring of CA3: Indications for connectional heterogeneityPreprint
Witter, M. P. (2007) · Learning & Memory · doi:10.1101/lm.725207 · Cited by 234 · see citing works
From chemotaxis to the cognitive map: The function of olfaction
Jacobs, L. F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201880109 · Cited by 227 · see citing works
Neural Mechanisms of Self-Location
Barry, C., & Burgess, N. (2014) · Current Biology · doi:10.1016/j.cub.2014.02.049 · Cited by 168 · see citing works
Kemp, A., & Manahan‐Vaughan, D. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm136 · Cited by 154 · see citing works
Self-citationThe influence of objects on place field expression and size in distal hippocampal CA1
Burke, S. N., Maurer, A. P., Nematollahi, S., Uprety, A. R., Wallace, J. L., & Barnes, C. A. (2011) · Hippocampus · doi:10.1002/hipo.20929 · Cited by 130 · see citing works
Spatial Object Recognition Enables Endogenous LTD that Curtails LTP in the Mouse Hippocampus
Goh, J. J., & Manahan‐Vaughan, D. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs089 · Cited by 116 · see citing works
Self-citationNakamura, N. H., Flasbeck, V., Maingret, N., Kitsukawa, T., & Sauvage, M. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4480-12.2013 · Cited by 103 · see citing works
Jacobs, L. F., & Menzel, R. (2014) · Movement Ecology · doi:10.1186/2051-3933-2-3 · Cited by 99 · see citing works
Cellular Compartment Analysis of Temporal Activity by Fluorescence In Situ Hybridization (catFISH)
Guzowski, J. F., & Worley, P. F. (2001) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0108s15 · Cited by 86 · see citing works
Hagena, H., & Manahan‐Vaughan, D. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq271 · Cited by 84 · see citing works
Self-citationFunctional division of hippocampal area CA1 via modulatory gating of entorhinal cortical inputs
Ito, H., & Schuman, E. M. (2011) · Hippocampus · doi:10.1002/hipo.20909 · Cited by 79 · see citing works
Tamamaki, N. (1997) · Experimental Brain Research · doi:10.1007/pl00005753 · Cited by 74 · see citing works
Hagena, H., & Manahan‐Vaughan, D. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00023 · Cited by 47 · see citing works
Self-citationMapping memory function in the medial temporal lobe with the immediate-early gene Arc
Sauvage, M. M., Nakamura, N. H., & Beer, Z. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.048 · Cited by 41 · see citing works
Spatial olfactory learning facilitates long‐term depression in the hippocampus
André, M. A. E., & Manahan‐Vaughan, D. (2013) · Hippocampus · doi:10.1002/hipo.22158 · Cited by 33 · see citing works
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Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
- Authors
- Hoang, T., Aliane, V., & Manahan‐Vaughan, D.
- Affiliations
- Ruhr University Bochum (DE)
- Corresponding author
- Manahan‐Vaughan, Denise
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2018-02-19
- Volume
- 28
- Issue
- 5
- Pages
- 315-326
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC5947642
- OpenAlex
- W2793966431
- Cited by
- 37
- References
- 42
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 2 · 2023: 2 · 2022: 8 · 2021: 7 · 2020: 4 · 2019: 5 · 2018: 4
- FWCI
- 2.97
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Hippocampus (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- German Research Foundation (SFB874/B1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampal subfields, spatial coding, positional cues, directional cues, CA1, dentate gyrus, CA3, immediate early genes, Arc, Homer1a, spatial navigation
- MeSH terms
- Homer Scaffolding Proteins, Animals, Cues, Cytoskeletal Proteins, Exploratory Behavior, Gene Expression Regulation, Hippocampus, Male, Memory, Short-Term, Nerve Tissue Proteins, Neurons, Orientation, Space Perception, Rats, Wistar, In Situ Hybridization, Fluorescence, Long-Term Synaptic Depression, Memory, Long-Term, Spatial Memory, Spatial Processing
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