Silent Learning

Janine I. Rossato; Andrea Moreno; Lisa Genzel; Miwako Yamasaki; Tomonori Takeuchi; Santiago Canals; Richard G.M. Morris

doi:10.1016/j.cub.2018.09.012

Silent Learning

Janine I. Rossato, Andrea Moreno, Lisa Genzel, Miwako Yamasaki, Tomonori Takeuchi, Santiago Canals, Richard G.M. Morris

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

We introduce the concept of “silent learning”—the capacity to learn despite neuronal cell-firing being largely absent. This idea emerged from thinking about dendritic computation [1, 2] and examining whether the encoding, expression, and retrieval of hippocampal-dependent memory could be dissociated using the intrahippocampal infusion of pharmacological compounds. We observed that very modest enhancement of GABAergic inhibition with low-dose muscimol blocked both cell-firing and the retrieval of an already-formed memory but left induction of long-term potentiation (LTP) and new spatial memory encoding intact (silent learning). In contrast, blockade of hippocampal NMDA receptors by intrahippocampal D-AP5 impaired both the induction of LTP and encoding but had no effect on memory retrieval. Blockade of AMPA receptors by CNQX impaired excitatory synaptic transmission and cell-firing and both memory encoding and retrieval. Thus, in keeping with the synaptic plasticity and memory hypothesis [3], the hippocampal network can mediate new memory encoding when LTP induction is intact even under conditions in which somatic cell-firing is blocked. It is widely believed that induction of long-term potentiation (LTP) and associated cell-firing is required for new memory formation. Rossato et al. show that memory formation can still occur provided LTP induction is intact even though cell-firing has been prevented using modest GABAergic activation. We refer to this as “silent learning.”

Original language	English
Journal	Current Biology
Volume	28
Issue	21
Pages (from-to)	3508-3515
Number of pages	8
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2018.09.012
Publication status	Published - 2018

Keywords

AMPA receptors
GABA receptors
NMDA receptors
learning
long-term potentiation
memory encoding
memory retrieval
synaptic plasticity
watermaze
NMDA RECEPTORS
ON-DEMAND PLATFORM
ASPARTATE RECEPTOR ANTAGONIST
SYNAPTIC PLASTICITY
WATER-MAZE PROCEDURE
DORSAL HIPPOCAMPUS
SELECTIVE IMPAIRMENT
PLACE FIELDS
SPATIAL MEMORY
LONG-TERM POTENTIATION

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10.1016/j.cub.2018.09.012

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title = "Silent Learning",

abstract = "We introduce the concept of “silent learning”—the capacity to learn despite neuronal cell-firing being largely absent. This idea emerged from thinking about dendritic computation [1, 2] and examining whether the encoding, expression, and retrieval of hippocampal-dependent memory could be dissociated using the intrahippocampal infusion of pharmacological compounds. We observed that very modest enhancement of GABAergic inhibition with low-dose muscimol blocked both cell-firing and the retrieval of an already-formed memory but left induction of long-term potentiation (LTP) and new spatial memory encoding intact (silent learning). In contrast, blockade of hippocampal NMDA receptors by intrahippocampal D-AP5 impaired both the induction of LTP and encoding but had no effect on memory retrieval. Blockade of AMPA receptors by CNQX impaired excitatory synaptic transmission and cell-firing and both memory encoding and retrieval. Thus, in keeping with the synaptic plasticity and memory hypothesis [3], the hippocampal network can mediate new memory encoding when LTP induction is intact even under conditions in which somatic cell-firing is blocked. It is widely believed that induction of long-term potentiation (LTP) and associated cell-firing is required for new memory formation. Rossato et al. show that memory formation can still occur provided LTP induction is intact even though cell-firing has been prevented using modest GABAergic activation. We refer to this as “silent learning.”",

keywords = "AMPA receptors, GABA receptors, NMDA receptors, learning, long-term potentiation, memory encoding, memory retrieval, synaptic plasticity, watermaze, NMDA RECEPTORS, ON-DEMAND PLATFORM, ASPARTATE RECEPTOR ANTAGONIST, SYNAPTIC PLASTICITY, WATER-MAZE PROCEDURE, DORSAL HIPPOCAMPUS, SELECTIVE IMPAIRMENT, PLACE FIELDS, SPATIAL MEMORY, LONG-TERM POTENTIATION",

author = "Rossato, {Janine I.} and Andrea Moreno and Lisa Genzel and Miwako Yamasaki and Tomonori Takeuchi and Santiago Canals and Morris, {Richard G.M.}",

note = "doi: 10.1016/j.cub.2018.09.012",

year = "2018",

doi = "10.1016/j.cub.2018.09.012",

language = "English",

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TY - JOUR

T1 - Silent Learning

AU - Rossato, Janine I.

AU - Moreno, Andrea

AU - Genzel, Lisa

AU - Yamasaki, Miwako

AU - Takeuchi, Tomonori

AU - Canals, Santiago

AU - Morris, Richard G.M.

N1 - doi: 10.1016/j.cub.2018.09.012

PY - 2018

Y1 - 2018

N2 - We introduce the concept of “silent learning”—the capacity to learn despite neuronal cell-firing being largely absent. This idea emerged from thinking about dendritic computation [1, 2] and examining whether the encoding, expression, and retrieval of hippocampal-dependent memory could be dissociated using the intrahippocampal infusion of pharmacological compounds. We observed that very modest enhancement of GABAergic inhibition with low-dose muscimol blocked both cell-firing and the retrieval of an already-formed memory but left induction of long-term potentiation (LTP) and new spatial memory encoding intact (silent learning). In contrast, blockade of hippocampal NMDA receptors by intrahippocampal D-AP5 impaired both the induction of LTP and encoding but had no effect on memory retrieval. Blockade of AMPA receptors by CNQX impaired excitatory synaptic transmission and cell-firing and both memory encoding and retrieval. Thus, in keeping with the synaptic plasticity and memory hypothesis [3], the hippocampal network can mediate new memory encoding when LTP induction is intact even under conditions in which somatic cell-firing is blocked. It is widely believed that induction of long-term potentiation (LTP) and associated cell-firing is required for new memory formation. Rossato et al. show that memory formation can still occur provided LTP induction is intact even though cell-firing has been prevented using modest GABAergic activation. We refer to this as “silent learning.”

AB - We introduce the concept of “silent learning”—the capacity to learn despite neuronal cell-firing being largely absent. This idea emerged from thinking about dendritic computation [1, 2] and examining whether the encoding, expression, and retrieval of hippocampal-dependent memory could be dissociated using the intrahippocampal infusion of pharmacological compounds. We observed that very modest enhancement of GABAergic inhibition with low-dose muscimol blocked both cell-firing and the retrieval of an already-formed memory but left induction of long-term potentiation (LTP) and new spatial memory encoding intact (silent learning). In contrast, blockade of hippocampal NMDA receptors by intrahippocampal D-AP5 impaired both the induction of LTP and encoding but had no effect on memory retrieval. Blockade of AMPA receptors by CNQX impaired excitatory synaptic transmission and cell-firing and both memory encoding and retrieval. Thus, in keeping with the synaptic plasticity and memory hypothesis [3], the hippocampal network can mediate new memory encoding when LTP induction is intact even under conditions in which somatic cell-firing is blocked. It is widely believed that induction of long-term potentiation (LTP) and associated cell-firing is required for new memory formation. Rossato et al. show that memory formation can still occur provided LTP induction is intact even though cell-firing has been prevented using modest GABAergic activation. We refer to this as “silent learning.”

KW - AMPA receptors

KW - GABA receptors

KW - NMDA receptors

KW - learning

KW - long-term potentiation

KW - memory encoding

KW - memory retrieval

KW - synaptic plasticity

KW - watermaze

KW - NMDA RECEPTORS

KW - ON-DEMAND PLATFORM

KW - ASPARTATE RECEPTOR ANTAGONIST

KW - SYNAPTIC PLASTICITY

KW - WATER-MAZE PROCEDURE

KW - DORSAL HIPPOCAMPUS

KW - SELECTIVE IMPAIRMENT

KW - PLACE FIELDS

KW - SPATIAL MEMORY

KW - LONG-TERM POTENTIATION

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U2 - 10.1016/j.cub.2018.09.012

DO - 10.1016/j.cub.2018.09.012

M3 - Journal article

C2 - 30415706

SN - 0960-9822

VL - 28

SP - 3508

EP - 3515

JO - Current Biology

JF - Current Biology

IS - 21

ER -

Silent Learning

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