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Hippocampal electrical stimulation disrupts associative learning when targeted at dentate spikes

Year of publication

2017

Authors

Nokia, Miriam; Gureviciene, Irina; Waselius, Tomi; Tanila, Heikki; Penttonen, Markku

Abstract

Hippocampal electrophysiological oscillations, namely theta and ripples, have been implicated in encoding and consolidation of new memories, respectively. According to existing literature, hippocampal dentate spikes are prominent, short‐duration (<30 ms), large‐amplitude (∼2–4 mV) fluctuations in hilar local‐field potentials that take place during awake immobility and sleep. Interestingly, previous studies indicate that during dentate spikes dentate gyrus granule cells increase their firing while firing of CA1 pyramidal cells are suppressed, thus resulting in momentary uncoupling of the two hippocampal subregions. To date, the behavioural significance of dentate spikes is unknown. Here, to study the possible role of dentate spikes in learning, we trained adult male Sprague–Dawley rats in trace eyeblink classical conditioning. For 1 h immediately following each conditioning session, one group of animals received hippocampal stimulation via the ventral hippocampal commissure (vHC) contingent on dentate spikes to disrupt the uncoupling between the dentate gyrus and the CA1 subregions. A yoked control group was stimulated during immobility, irrespective of brain state, and another control group was not stimulated at all. As a result, learning was impaired only in the group where vHC stimulation was administered contingent on dentate spikes. Our results suggest dentate spikes and/or the associated uncoupling of the dentate gyrus and the CA1 play a significant role in memory consolidation. Dentate spikes could possibly reflect reactivation and refinement of a memory trace within the dentate gyrus triggered by input from the entorhinal cortex.
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Organizations and authors

University of Eastern Finland

Tanila Heikki

Gureviciene Irina

University of Jyväskylä

Gureviciene Irina

Penttonen Markku Orcid -palvelun logo

Nokia Miriam Orcid -palvelun logo

Waselius Tomi Orcid -palvelun logo

Publication type

Publication format

Article

Parent publication type

Journal

Article type

Original article

Audience

Scientific

Peer-reviewed

Peer-Reviewed

MINEDU's publication type classification code

A1 Journal article (refereed), original research

Publication channel information

Volume

595

Issue

14

Article number

10.1113/JP274023

Pages

4961-4971

​Publication forum

61368

​Publication forum level

3

Open access

Open access in the publisher’s service

No

Self-archived

Yes

Other information

Fields of science

Psychology; Neurosciences

Keywords

[object Object]

Internationality of the publisher

International

International co-publication

No

Co-publication with a company

No

DOI

10.1113/JP274023

The publication is included in the Ministry of Education and Culture’s Publication data collection

Yes