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UCSD COGS 107B - Topographic Specificity

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Topographic specificity of functional connections from hippocampal CA3 to CA1Iman H. Brivanlou, Jami L. M. Dantzker, Charles F. Stevens, and Edward M. Callaway doi:10.1073/pnas.0308577100 2004;101;2560-2565; originally published online Feb 10, 2004; PNAS This information is current as of January 2007. & ServicesOnline Information www.pnas.org/cgi/content/full/101/8/2560etc., can be found at: High-resolution figures, a citation map, links to PubMed and Google Scholar, References www.pnas.org/cgi/content/full/101/8/2560#BIBLThis article cites 17 articles, 4 of which you can access for free at: www.pnas.org/cgi/content/full/101/8/2560#otherarticlesThis article has been cited by other articles: E-mail Alerts. click hereat the top right corner of the article orReceive free email alerts when new articles cite this article - sign up in the box Rights & Permissions www.pnas.org/misc/rightperm.shtmlTo reproduce this article in part (figures, tables) or in entirety, see: Reprints www.pnas.org/misc/reprints.shtmlTo order reprints, see: Notes:Topographic specificity of functional connectionsfrom hippocampal CA3 to CA1Iman H. Brivanlou*, Jami L. M. Dantzker†, Charles F. Stevens*‡, and Edward M. Callaway§*Molecular Neurobiology Laboratory, Howard Hughes Medical Institute, and§Systems Neurobiology Laboratory, The Salk Institute, 10010 North TorreyPines Road, La Jolla, CA 92037; and†Howard Hughes Medical Institute, Department of Anatomy, University of California, San Francisco, CA 94143-0452Contributed by Charles F. Stevens, December 22, 2003The hippocampus is a cortical region thought to play an importantrole in learning and memory. Most of our knowledge about thedetailed organization of hippocampal circuitry responsible forthese functions is derived from anatomical studies. These studiespresent an incomplete picture, however, because the functionalcharacter and importance of connections are often not revealed byanatomy. Here, we used a physiological method (photostimulationwith caged glutamate) to probe the fine pattern of functionalconnectivity between the CA3 and CA1 subfields in the mousehippocampal slice preparation. We recorded intracellularly fromCA1 and CA3 pyramidal neurons while scanning with photostimu-lation across the entire CA3 subfield with high spatial resolution.Our results show that, at a given septotemporal level, nearby CA1neurons receive synaptic inputs from neighboring CA3 neurons.Thus, the CA3 to CA1 mapping preserves neighbor relations.The concept of cortical maps plays a central role in ourunderstanding of cortical function. Many, if not all, corticalareas are organized according to some sort of map, and this fact,together with the idea that the hippocampus contains a ‘‘cog-nitive map’’ (1), naturally leads to the idea that the hippocampusmight have a map-like organization. The existence of such anhippocampal map would be important for understanding thefunction of this important structure (2) because knowing what isrepresented in the map, and how this representation is arranged,would place constraints on what computations the hippocampuscould carry out. Whatever arrangement a hippocampal mapmight have, the very idea of a map involves a knowledge of thebasic intracortical circuitry, and of the topological arrangementof that circuitry. Our goal here is to investigate the topology ofhippocampal CA3 to CA1 mapping. That is, we wish to deter-mine the extent to which neighbor relations in CA3 are preservedin the projections to CA1.To place our goals in context, we need to review briefly thecurrent understanding of hippocampal organization as revealedby anatomical and physiological methods.Most of our knowledge about the detailed organization andconnectivity of circuits within the hippocampus is derived fromextensive anatomical studies (3–11). The pioneering works ofRamon y Cajal and Lorente de No established that the fields ofthe hippocampal formation are linked by a sequence of uniqueand largely unidirectional connections, the fundamental ‘‘tri-synaptic circuit’’: The dentate gyrus receives its major input fromthe entorhinal cortex via the so-called perforant path. Thegranule cells of the dentate gyrus project via the mossy fibers tothe CA3 field of the hippocampus. Pyramidal cells of the CA3field in turn give rise to collateralized axons, the Schaffercollaterals, that terminate within CA3 as associational connec-tions and also provide a major input to the CA1 field.Andersen and colleagues proposed an important extension ofthis basic tri-synaptic circuit concept: according to their view, thehippocampus is organized in parallel ‘‘lamellae,’’ or small stripsor slices (4); this is the so-called ‘‘lamellar hypothesis.’’ Thelamellar hypothesis formed a conceptual basis for the use of thein vitro hippocampal slice preparation as a means of studyingsynaptic physiology because all components of the tri-synaptichippocampal circuit would be contained in an easily isolated sliceamenable to manipulation and study. The lamellar hypothesiswas, however, revisited by Amaral and colleagues (5, 8) andfound to be an incomplete description of hippocampal connec-tivity because Schaffer collateral projections from CA3 to CA1were shown to provide a wide dispersion of information from aparticular level in the hippocampus to much of its septotemporalextent.Anatomical studies have shown that the projections from CA3to CA1 are, however, far from random. Rather, the generaltarget area in CA1 for a given CA3 neuron depends on the thatneuron’s septotemporal and transverse position within the CA3cortical sheet (7, 8). Most relevant for the present work is theobservation that the CA1 map is ‘‘flipped’’ in the transversedirection relative to the CA3 map so that CA3 neurons nearestCA1 tend to project to the closest CA1 neurons, and CA3neurons farthest from CA1 tend to project to the most trans-versely distant CA1 cells. Here, we confirm and extend thisanatomical observation by showing, with a functional method,that the flipped mapping is topological in the sense that neigh-bors in CA3 project to neighbors in CA1.Physiological studies of hippocampal activity and the func-tional correlates of neural firing (1, 12, 13) have provided furtherimportant clues to the organization of hippocampal circuits.These studies have shown that the activity of hippocampalpyramidal neurons in rodents exploring the environment ischaracterized by ‘‘place fields,’’


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UCSD COGS 107B - Topographic Specificity

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