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Phencyclidine discoordinates hippocampal network activity but not place fields

Hsin-Yi Kao, Dino Dvořák, EunHye Park, Jana Kenney, Eduard Kelemen, André A Fenton
doi: https://doi.org/10.1101/200162
Hsin-Yi Kao
1Graduate Program in Neural and Behavioral Science, State University of New York, Downstate Medical Center
2Department of Physiology and Pharmacology, State University of New York, Downstate Medical Center
3Center for Neural Science, New York University
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Dino Dvořák
2Department of Physiology and Pharmacology, State University of New York, Downstate Medical Center
3Center for Neural Science, New York University
4Joint Graduate Program in Biomedical Engineering State University of New York, Downstate Medical Center and New York University/Polytechnic University
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EunHye Park
3Center for Neural Science, New York University
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Jana Kenney
5Institute of Physiology, Czech Academy of Sciences, Prague, Czech Republic
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Eduard Kelemen
1Graduate Program in Neural and Behavioral Science, State University of New York, Downstate Medical Center
2Department of Physiology and Pharmacology, State University of New York, Downstate Medical Center
6National Institute of Mental Health, Klecany, Czech Republic
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André A Fenton
2Department of Physiology and Pharmacology, State University of New York, Downstate Medical Center
3Center for Neural Science, New York University
7The Robert F. Furchgott Center for Neural & Behavioral Science, State University of New York, Downstate Medical Center, Brooklyn, New York, USA
8Neuroscience Institute at the New York University Langone Medical Center
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  • For correspondence: afenton@nyu.edu
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ABSTRACT

We used the psychotomimetic phencyclidine (PCP) to investigate the relationships between cognitive behavior, coordinated neural network function and information processing within the hippocampus place cell system. We report in rats that PCP (5mg/kg i.p.) impairs a well-learned hippocampus-dependent place avoidance behavior in rats that requires cognitive control, even when PCP is injected directly into dorsal hippocampus. PCP increases 60-100 Hz medium gamma oscillations in hippocampus CA1 and these increases correlate with the cognitive impairment caused by systemic PCP administration. PCP discoordinates theta-modulated medium and slow gamma oscillations in CA1 local field potentials (LFP) such that medium gamma oscillations become more theta-organized than slow gamma oscillations. CA1 place cell firing fields are preserved under PCP but the drug discoordinates the sub-second temporal organization of discharge amongst place cells. This discoordination causes place cell ensemble representations of a familiar space to cease resembling pre-PCP representations, despite preserved place fields. These findings point to the cognitive impairments caused by PCP arising from neural discoordination. PCP disrupts the timing of discharge with respect to the sub-second timescales of theta and gamma oscillations in the LFP. Because these oscillations arise from local inhibitory synaptic activity, these findings point to excitation-inhibition discoordination as the root of PCP-induced cognitive impairment.

SIGNIFICANCE STATEMENT Hippocampal neural discharge is temporally coordinated on timescales of theta and gamma oscillations in the local field potential, and the discharge of a subset of pyramidal neurons called “place cells” is spatially organized such that discharge is restricted to locations called a cell’s “place field.” Because this temporal coordination and spatial discharge organization is thought to represent spatial knowledge, we used the psychotomimetic phencyclidine (PCP) to disrupt cognitive behavior and assess the importance of neural coordination and place fields for spatial cognition. PCP impaired the judicious use of spatial information and discoordinated hippocampal discharge, without disrupting firing fields. These findings dissociate place fields from spatial cognitive behavior and suggest that hippocampus discharge coordination is crucial to spatial cognition.

Footnotes

  • FINANCIAL DISCLOSURES: The authors declare there are no competing financial or non-financial interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 09, 2017.
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Phencyclidine discoordinates hippocampal network activity but not place fields
Hsin-Yi Kao, Dino Dvořák, EunHye Park, Jana Kenney, Eduard Kelemen, André A Fenton
bioRxiv 200162; doi: https://doi.org/10.1101/200162
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Phencyclidine discoordinates hippocampal network activity but not place fields
Hsin-Yi Kao, Dino Dvořák, EunHye Park, Jana Kenney, Eduard Kelemen, André A Fenton
bioRxiv 200162; doi: https://doi.org/10.1101/200162

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