Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1
Stefan Leutgeb,1
Jill K. Leutgeb,1
Alessandro Treves,1,2
May-Britt Moser,1
Edvard I. Moser1*
Abstract:
The hippocampus has differentiated into an extensively connectedrecurrent stage (CA3) followed by a feed-forward stage (CA1).We examined the function of this structural differentiationby determining how cell ensembles in rat CA3 and CA1 generaterepresentations of rooms with common spatial elements. In CA3,distinct subsets of pyramidal cells were activated in each room,regardless of the similarity of the testing enclosure. In CA1,the activated populations overlapped, and the overlap increasedin similar enclosures. After exposure to a novel room, ensembleactivity developed slower in CA3 than CA1, suggesting that therepresentations emerged independently.
1 Centre for the Biology of Memory, Medical-Technical Research Centre, Norwegian University of Science and Technology, 7489 Trondheim, Norway. 2 Cognitive Neuroscience Sector, International School for Advanced Studies, Trieste, Italy.
Note added in proof: Additional evidence for CA1-CA3 differencesis provided by a recent study measuring immediate early geneactivation in two different novel rooms (36).
* To whom correspondence should be addressed. E-mail: edvard.moser{at}cbm.ntnu.no
The editors suggest the following Related Resources on Science sites:
In Science Magazine
PERSPECTIVES
David K. Bilkey (27 August 2004) Science305 (5688), 1245.
[DOI: 10.1126/science.1102895] |Summary »|Full Text »|PDF »
Evidence for Encoding versus Retrieval Scheduling in the Hippocampus by Theta Phase and Acetylcholine.
V. Douchamps, A. Jeewajee, P. Blundell, N. Burgess, and C. Lever (2013)
J. Neurosci.
33, 8689-8704
|Abstract »|Full Text »|PDF »
Distinct Dendritic Arborization and In Vivo Firing Patterns of Parvalbumin-Expressing Basket Cells in the Hippocampal Area CA3.
J. J. Tukker, B. Lasztoczi, L. Katona, J. D. B. Roberts, E. K. Pissadaki, Y. Dalezios, L. Marton, L. Zhang, T. Klausberger, and P. Somogyi (2013)
J. Neurosci.
33, 6809-6825
|Abstract »|Full Text »|PDF »
Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice.
Reward Cues in Space: Commonalities and Differences in Neural Coding by Hippocampal and Ventral Striatal Ensembles.
C. S. Lansink, J. C. Jackson, J. V. Lankelma, R. Ito, T. W. Robbins, B. J. Everitt, and C. M. A. Pennartz (2012)
J. Neurosci.
32, 12444-12459
|Abstract »|Full Text »|PDF »
Spatial Information Outflow from the Hippocampal Circuit: Distributed Spatial Coding and Phase Precession in the Subiculum.
S. M. Kim, S. Ganguli, and L. M. Frank (2012)
J. Neurosci.
32, 11539-11558
|Abstract »|Full Text »|PDF »
Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task.
P. M. Itskov, E. Vinnik, C. Honey, J. Schnupp, and M. E. Diamond (2012)
J Neurophysiol
107, 1822-1834
|Abstract »|Full Text »|PDF »
Hippocampal Dynamics Predict Interindividual Cognitive Differences in Rats.
V. Hok, E. Chah, R. B. Reilly, and S. M. O'Mara (2012)
J. Neurosci.
32, 3540-3551
|Abstract »|Full Text »|PDF »
Remembering to Learn: Independent Place and Journey Coding Mechanisms Contribute to Memory Transfer.
Age-related memory deficits linked to circuit-specific disruptions in the hippocampus.
M. A. Yassa, A. T. Mattfeld, S. M. Stark, and C. E. L. Stark (2011)
PNAS
108, 8873-8878
|Abstract »|Full Text »|PDF »
Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity.
J. W. Lacy, M. A. Yassa, S. M. Stark, L. T. Muftuler, and C. E. L. Stark (2010)
Learn. Mem.
18, 15-18
|Abstract »|Full Text »|PDF »
Experience-Dependent Development of Coordinated Hippocampal Spatial Activity Representing the Similarity of Related Locations.
A. C. Singer, M. P. Karlsson, A. R. Nathe, M. F. Carr, and L. M. Frank (2010)
J. Neurosci.
30, 11586-11604
|Abstract »|Full Text »|PDF »
Attractor-Map Versus Autoassociation Based Attractor Dynamics in the Hippocampal Network.
L. L. Colgin, S. Leutgeb, K. Jezek, J. K. Leutgeb, E. I. Moser, B. L. McNaughton, and M.-B. Moser (2010)
J Neurophysiol
104, 35-50
|Abstract »|Full Text »|PDF »
Individual differences in spatial pattern separation performance associated with healthy aging in humans.
S. M. Stark, M. A. Yassa, and C. E. L. Stark (2010)
Learn. Mem.
17, 284-288
|Abstract »|Full Text »|PDF »
Hebbian Analysis of the Transformation of Medial Entorhinal Grid-Cell Inputs to Hippocampal Place Fields.
Attention-Like Modulation of Hippocampus Place Cell Discharge.
A. A. Fenton, W. W. Lytton, J. M. Barry, P. P. Lenck-Santini, L. E. Zinyuk, S. Kubik, J. Bures, B. Poucet, R. U. Muller, and A. V. Olypher (2010)
J. Neurosci.
30, 4613-4625
|Abstract »|Full Text »|PDF »
Mitochondrial DNA Toxicity in Forebrain Neurons Causes Apoptosis, Neurodegeneration, and Impaired Behavior.
K. H. Lauritzen, O. Moldestad, L. Eide, H. Carlsen, G. Nesse, J. F. Storm, I. M. Mansuy, L. H. Bergersen, and A. Klungland (2010)
Mol. Cell. Biol.
30, 1357-1367
|Abstract »|Full Text »|PDF »
Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events.
Accuracy of hippocampal network activity is disrupted by neuroinflammation: rescue by memantine.
S. Rosi, V. Ramirez-Amaya, A. Vazdarjanova, E. E. Esparza, P. B. Larkin, J. R. Fike, G. L. Wenk, and C. A. Barnes (2009)
Brain
132, 2464-2477
|Abstract »|Full Text »|PDF »
A Code for Spatial Alternation During Fixation in Rat Hippocampal CA1 Neurons.
M. Takahashi, J. Lauwereyns, Y. Sakurai, and M. Tsukada (2009)
J Neurophysiol
102, 556-567
|Abstract »|Full Text »|PDF »
The Multiple Origins and Laminar Topography of the Hippocampal Theta Rhythm.
P. Shirvalkar and A. S. Bahar (2009)
J. Neurosci.
29, 7111-7113
|Full Text »|PDF »
Visual object pattern separation deficits in nondemented older adults.
C. K. Toner, E. Pirogovsky, C. B. Kirwan, and P. E. Gilbert (2009)
Learn. Mem.
16, 338-342
|Abstract »|Full Text »|PDF »
A Specific Role of the Human Hippocampus in Recall of Temporal Sequences.
H. Lehn, H.-A. Steffenach, N. M. van Strien, D. J. Veltman, M. P. Witter, and A. K. Haberg (2009)
J. Neurosci.
29, 3475-3484
|Abstract »|Full Text »|PDF »
Vasopressin 1b Receptor Knock-Out Impairs Memory for Temporal Order.
L. M. DeVito, R. Konigsberg, C. Lykken, M. Sauvage, W. S. Young III, and H. Eichenbaum (2009)
J. Neurosci.
29, 2676-2683
|Abstract »|Full Text »|PDF »
Network Dynamics Underlying the Formation of Sparse, Informative Representations in the Hippocampus.
Rapid encoding of new information alters the profile of plasticity-related mRNA transcripts in the hippocampal CA3 region.
R. P. Haberman, H. J. Lee, C. Colantuoni, M. T. Koh, and M. Gallagher (2008)
PNAS
105, 10601-10606
|Abstract »|Full Text »|PDF »
Finite Scale of Spatial Representation in the Hippocampus.
K. B. Kjelstrup, T. Solstad, V. H. Brun, T. Hafting, S. Leutgeb, M. P. Witter, E. I. Moser, and M.-B. Moser (2008)
Science
321, 140-143
|Abstract »|Full Text »|PDF »
Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory.
J. J. Kim, H. J. Lee, A. C. Welday, E. Song, J. Cho, P. E. Sharp, M. W. Jung, and H. T. Blair (2007)
PNAS
104, 18297-18302
|Abstract »|Full Text »|PDF »
Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point.
Dentate Gyrus NMDA Receptors Mediate Rapid Pattern Separation in the Hippocampal Network.
T. J. McHugh, M. W. Jones, J. J. Quinn, N. Balthasar, R. Coppari, J. K. Elmquist, B. B. Lowell, M. S. Fanselow, M. A. Wilson, and S. Tonegawa (2007)
Science
317, 94-99
|Abstract »|Full Text »|PDF »
Recruitment of an inhibitory hippocampal network after bursting in a single granule cell.
The Role of CA3 Hippocampal NMDA Receptors in Paired Associate Learning.
T. Rajji, D. Chapman, H. Eichenbaum, and R. Greene (2006)
J. Neurosci.
26, 908-915
|Abstract »|Full Text »|PDF »
Hippocampal CA1 Circuitry Dynamically Gates Direct Cortical Inputs Preferentially at Theta Frequencies.
C. W. Ang, G. C. Carlson, and D. A. Coulter (2005)
J. Neurosci.
25, 9567-9580
|Abstract »|Full Text »|PDF »
Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation.
P. A. Gusev, C. Cui, D. L. Alkon, and A. N. Gubin (2005)
J. Neurosci.
25, 9384-9397
|Abstract »|Full Text »|PDF »
Behavioral Evidence That Segregation and Representation Are Dissociable Hippocampal Functions.