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The Journal of Neuroscience, December 27, 2006, 26(52):13485-13492; doi:10.1523/JNEUROSCI.2882-06.2006

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Behavioral/Systems/Cognitive
Phase Precession in Hippocampal Interneurons Showing Strong Functional Coupling to Individual Pyramidal Cells

Andrew P. Maurer, Stephen L. Cowen, Sara N. Burke, Carol A. Barnes, and Bruce L. McNaughton

Arizona Research Laboratories Division of Neural Systems, Memory and Aging, University of Arizona, Tucson, Arizona 85724

Correspondence should be addressed to Bruce L. McNaughton, Neural Systems, Memory, and Aging Division, Life Sciences North Building, Room 384, University of Arizona, Tucson, AZ 85724. Email: bruce{at}nsma.arizona.edu

Although hippocampal interneurons typically do not show discrete regions of elevated firing in an environment, such as seen in pyramidal cell place fields, they do exhibit significant spatial modulation (McNaughton et al., 1983a). Strong monosynaptic coupling between pyramidal neurons and nearby interneurons in the CA1 stratum pyramidale has been strongly implicated on the basis of significant, short-latency peaks in cross-correlogram plots (Csicsvari et al., 1998). Furthermore, interneurons receiving a putative monosynaptic connection from a simultaneously recorded pyramidal cell appear to inherit the spatial modulation of the latter (Marshall et al., 2002). Buzsaki and colleagues hypothesize that interneurons may also adopt the firing phase dynamics of their afferent place cells, which show a phase shift relative to the hippocampal theta rhythm as a rat passes through the place field ("phase precession"). This study confirms and extends the previous reports by showing that interneurons in the dorsal and middle hippocampus with putative monosynaptic connections with place cells recorded on the same tetrode share other properties with their pyramidal cell afferents, including the spatial scale of the place field of pyramidal cell, a characteristic of the septotemporal level of the hippocampus from which the cells are recorded, and the rate of phase precession, which is slower in middle regions. Furthermore, variations in pyramidal cell place field scale within each septotemporal level attributable to task variations are similarly associated with variations in interneuron place field scale. The available data strongly suggest that spatial selectivity of CA1 stratum pyramidale interneurons is inherited from a small cluster of local pyramidal cells and is not a consequence of spatially selective synaptic input from CA3 or other sources.

Key words: hippocampus; oscillation; place cell; rat; theta rhythm; place field

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Received July 7, 2006; revised Oct. 20, 2006; accepted Nov. 15, 2006.

Correspondence should be addressed to Bruce L. McNaughton, Neural Systems, Memory, and Aging Division, Life Sciences North Building, Room 384, University of Arizona, Tucson, AZ 85724. Email: bruce{at}nsma.arizona.edu

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