Mechanisms for Selective Single-Cell Reactivation during Offline Sharp-Wave Ripples and Their Distortion by Fast Ripples

Memory traces are reactivated selectively during sharp-wave ripples. The mechanisms of selective reactivation, and how degraded reactivation affects memory, are poorly understood. We evaluated hippocampal single-cell activity during physiological and pathological sharp-wave ripples using juxtacellul...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2017-06, Vol.94 (6), p.1234-1247.e7
Main Authors: Valero, Manuel, Averkin, Robert G., Fernandez-Lamo, Ivan, Aguilar, Juan, Lopez-Pigozzi, Diego, Brotons-Mas, Jorge R., Cid, Elena, Tamas, Gabor, Menendez de la Prida, Liset
Format: Article
Language:English
Subjects:
Action Potentials - drug effects
Action Potentials - physiology
Activation
Animals
Anticonvulsants - pharmacology
Brain Waves - drug effects
CA1 Region, Hippocampal - cytology
CA1 Region, Hippocampal - drug effects
CA1 Region, Hippocampal - physiopathology
Carbamazepine - pharmacology
Disease Models, Animal
Electroencephalography
Entropy
Epilepsy
Epilepsy - physiopathology
Epilepsy, Temporal Lobe - physiopathology
Epilepsy, Temporal Lobe - psychology
Firing
Hippocampus
Hippocampus - cytology
Hippocampus - drug effects
Hippocampus - physiopathology
Memory - drug effects
Memory Disorders - physiopathology
Memory Disorders - psychology
Memory, Episodic
Neural Inhibition
Neurology
Pyramidal cells
Pyramidal Cells - drug effects
Pyramidal Cells - physiology
Randomness
Rats
Rats, Wistar
Recognition (Psychology) - drug effects
Recognition (Psychology) - physiology
Ripples
Selectivity
Sleep
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Summary:Memory traces are reactivated selectively during sharp-wave ripples. The mechanisms of selective reactivation, and how degraded reactivation affects memory, are poorly understood. We evaluated hippocampal single-cell activity during physiological and pathological sharp-wave ripples using juxtacellular and intracellular recordings in normal and epileptic rats with different memory abilities. CA1 pyramidal cells participate selectively during physiological events but fired together during epileptic fast ripples. We found that firing selectivity was dominated by an event- and cell-specific synaptic drive, modulated in single cells by changes in the excitatory/inhibitory ratio measured intracellularly. This mechanism collapses during pathological fast ripples to exacerbate and randomize neuronal firing. Acute administration of a use- and cell-type-dependent sodium channel blocker reduced neuronal collapse and randomness and improved recall in epileptic rats. We propose that cell-specific synaptic inputs govern firing selectivity of CA1 pyramidal cells during sharp-wave ripples. •Unsupervised clustering discloses a mechanism of firing selectivity during ripples•Firing selectivity collapses in the epileptic hippocampus during fast ripples•Global and cell-specific synaptic drives are critical factors for selective firing•Tuning global and cell-specific factors allow improving recall in epileptic rats Valero et al. show how unsupervised clustering discloses a synaptic mechanism for CA1 firing selectivity during sharp-wave ripples. This mechanism is impaired in epileptic rats by collapsing cell-specific synaptic drives. This establishes new concepts in understanding selective neuronal firing.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2017.05.032