Behavioral state continuously modulates hippocampal information processing
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1
UCSF , United States
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2
Harvard University, Society of Fellows, United States
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3
Stanford University, Bioengineering, United States
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4
UCSF , Keck Center and Department of Physiology, United States
In behaving animals, changes in behavioral state are accompanied by profound changes in the patterns of recorded neural activity. In the rodent hippocampus, exploratory locomotion is associated with the prominent ~8Hz theta oscillation. Intervening periods of relative immobility (e.g., eating, grooming) are associated with high frequency (~200 Hz) sharp wave ripple (SWR) events. Studies involving the electrical microstimulation of hippocampal pathways have contributed to the conclusion that these states are separate both physiologically and functionally. Thus, the dominant view in the field is that theta governs a state where information is encoded in the hippocampal circuit while SWRs underlie a distinct state associated with consolidation. The presence of two clearly distinct states has not yet been proven, however. In addition, the effect of these states on the modulation of information transmission via the dentate gyrus (DG), a key pathway, has never been investigated in the intact animal. We used virally-mediated channelrhodopsin-2 (ChR2) to selectively activate the mossy fibers (MF), the dense projections from the dentate gyrus to hippocampal area CA3. Using an implanted optical fiber, we were able to activate the DG inputs to area CA3 while simultaneously recording downstream activity in behaving animals, including both single neuron spiking and LFPs. Histology revealed ChR2 expression limited to dentate granule cells and their processes, including strong expression in the mossy fibers. In recordings in CA3, repeated optical activation yielded a frequency facilitation effect further consistent with mossy fiber activation. We used low frequency (< 0.2 Hz) pulses at to probe the propagation of excitation along the trisynaptic pathway. Observing the output of this excitation in area CA1, we found that periods of fast movement corresponded to a large (nearly 50%) decrease in transmission. Moreover, we found that the modulation of information processing by behavior is not a switching between theta (moving) and SWR (still) states, but rather a continuum. This modulation manifested as a smooth reduction in fEPSP slope in CA1 as a function of increasing speed, where movement speed could account for up to 60%of the variance in EPSP slope. Intriguingly, the amplitude of SWRs in CA1 shows a similar speed-dependent decline; thus, as SC input is essential for normal CA1 SWRs, our results suggest that changes in the Schaeffer collateral synapse contribute to behaviorally dependent changes in CA1 output. Our results suggest that the simple two state model is not sufficient. Instead, they are consistent with the idea that that hippocampal information processing involves dynamic overlays of the integration of sensory information and more internally generated activity, with the balance shifting towards externally driven activation during locomotion and towards internal processing during stillness.
Conference:
Computational and Systems Neuroscience 2010, Salt Lake City, UT, United States, 25 Feb - 2 Mar, 2010.
Presentation Type:
Poster Presentation
Topic:
Poster session II
Citation:
Kemere
C,
Zhang
F,
Deisseroth
K and
Frank
LM
(2010). Behavioral state continuously modulates hippocampal information processing.
Front. Neurosci.
Conference Abstract:
Computational and Systems Neuroscience 2010.
doi: 10.3389/conf.fnins.2010.03.00211
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Received:
04 Mar 2010;
Published Online:
04 Mar 2010.
*
Correspondence:
Caleb Kemere, UCSF, Rijeka, United States, ckemere@gmail.com