Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior

Goal-directed behavior involves distributed neuronal circuits in the mammalian brain, including diverse regions of neocortex. However, the cellular basis of long-range cortico-cortical signaling during goal-directed behavior is poorly understood. Here, we recorded membrane potential of excitatory la...

Full description

Bibliographic Details
Main Authors: Takayuki Yamashita, Carl CH Petersen
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/15798
_version_ 1811181020314075136
author Takayuki Yamashita
Carl CH Petersen
author_facet Takayuki Yamashita
Carl CH Petersen
author_sort Takayuki Yamashita
collection DOAJ
description Goal-directed behavior involves distributed neuronal circuits in the mammalian brain, including diverse regions of neocortex. However, the cellular basis of long-range cortico-cortical signaling during goal-directed behavior is poorly understood. Here, we recorded membrane potential of excitatory layer 2/3 pyramidal neurons in primary somatosensory barrel cortex (S1) projecting to either primary motor cortex (M1) or secondary somatosensory cortex (S2) during a whisker detection task, in which thirsty mice learn to lick for water reward in response to a whisker deflection. Whisker stimulation in ‘Good performer’ mice, but not ‘Naive’ mice, evoked long-lasting biphasic depolarization correlated with task performance in S2-projecting (S2-p) neurons, but not M1-projecting (M1-p) neurons. Furthermore, S2-p neurons, but not M1-p neurons, became excited during spontaneous unrewarded licking in ‘Good performer’ mice, but not in ‘Naive’ mice. Thus, a learning-induced, projection-specific signal from S1 to S2 may contribute to goal-directed sensorimotor transformation of whisker sensation into licking motor output.
first_indexed 2024-04-11T09:11:20Z
format Article
id doaj.art-28ef946e3d6844c19d42d935a1e17247
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T09:11:20Z
publishDate 2016-06-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-28ef946e3d6844c19d42d935a1e172472022-12-22T04:32:29ZengeLife Sciences Publications LtdeLife2050-084X2016-06-01510.7554/eLife.15798Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behaviorTakayuki Yamashita0https://orcid.org/0000-0002-1849-9837Carl CH Petersen1https://orcid.org/0000-0003-3344-4495Laboratory of Sensory Processing, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland; Department of Neuroscience II, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanLaboratory of Sensory Processing, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandGoal-directed behavior involves distributed neuronal circuits in the mammalian brain, including diverse regions of neocortex. However, the cellular basis of long-range cortico-cortical signaling during goal-directed behavior is poorly understood. Here, we recorded membrane potential of excitatory layer 2/3 pyramidal neurons in primary somatosensory barrel cortex (S1) projecting to either primary motor cortex (M1) or secondary somatosensory cortex (S2) during a whisker detection task, in which thirsty mice learn to lick for water reward in response to a whisker deflection. Whisker stimulation in ‘Good performer’ mice, but not ‘Naive’ mice, evoked long-lasting biphasic depolarization correlated with task performance in S2-projecting (S2-p) neurons, but not M1-projecting (M1-p) neurons. Furthermore, S2-p neurons, but not M1-p neurons, became excited during spontaneous unrewarded licking in ‘Good performer’ mice, but not in ‘Naive’ mice. Thus, a learning-induced, projection-specific signal from S1 to S2 may contribute to goal-directed sensorimotor transformation of whisker sensation into licking motor output.https://elifesciences.org/articles/15798neocortical projection neuronsgoal-directed sensorimotor learningwhole-cell membrane potential recordingsprimary somatosensory barrel cortexsecondary somatosensory cortexwhisker motor cortex
spellingShingle Takayuki Yamashita
Carl CH Petersen
Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior
eLife
neocortical projection neurons
goal-directed sensorimotor learning
whole-cell membrane potential recordings
primary somatosensory barrel cortex
secondary somatosensory cortex
whisker motor cortex
title Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior
title_full Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior
title_fullStr Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior
title_full_unstemmed Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior
title_short Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior
title_sort target specific membrane potential dynamics of neocortical projection neurons during goal directed behavior
topic neocortical projection neurons
goal-directed sensorimotor learning
whole-cell membrane potential recordings
primary somatosensory barrel cortex
secondary somatosensory cortex
whisker motor cortex
url https://elifesciences.org/articles/15798
work_keys_str_mv AT takayukiyamashita targetspecificmembranepotentialdynamicsofneocorticalprojectionneuronsduringgoaldirectedbehavior
AT carlchpetersen targetspecificmembranepotentialdynamicsofneocorticalprojectionneuronsduringgoaldirectedbehavior