Sensory-evoked LTP driven by dendritic plateau potentials in vivo

• Published in: Nature (London) Vol. 515; no. 7525; pp. 116 - 119
• Main Authors: Gambino, Frédéric, Pagès, Stéphane, Kehayas, Vassilis, Baptista, Daniela, Tatti, Roberta, Carleton, Alan, Holtmaat, Anthony
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 06-11-2014; Nature Publishing Group
• Subjects: 14/35; 14/63; 14/69; 42/44; 631/378/1697/2604; 631/378/2591/2592; 631/378/2620/2623; 64/60; 9/10; 9/74; Action Potentials; Animals; Brain; Channelrhodopsins; Cognitive science; Dendrites - physiology; Evoked potentials (Electrophysiology); Humanities and Social Sciences; letter; Long-Term Potentiation; Male; Mice; Mice, Inbred C57BL; multidisciplinary; Neural transmission; Neurology; Neurons; Neuroscience; Physical Stimulation; Physiological aspects; Receptors, N-Methyl-D-Aspartate - metabolism; Rodents; Science; Signal transduction; Somatosensory Cortex - cytology; Somatosensory Cortex - physiology; Thalamus - cytology; Thalamus - physiology; Vibrissae - physiology; France
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature13664

Whole-cell recordings in mouse somatosensory cortex
in vivo
show that rhythmic sensory-whisker stimulation induces long-term synaptic potentiation (LTP) in layer 2/3 (L2/3) pyramidal cells, in the absence of somatic spikes, through long-lasting NMDAR-mediated depolarizations that are generated by synaptic networks originating from the posteromedial complex of the thalamus.
In vivo
synaptic LTP observed
Studies of synaptic plasticity mechanisms have predominantly been done
in vitro
, raising the question of which mechanisms are relevant to which systems
in vivo
. Recording from superficial neurons in mouse somatosensory cortex, Anthony Holtmaat and colleagues demonstrate that rhythmic sensory whisker stimulation induces long-term potentiation (LTP, a measure of cortical synaptic plasticity and memory formation) without the need for back-propagating action potentials from the cell body. Rather, LTP is dependent on the occurrence of long-lasting depolarizations within the dendrites. These data provide evidence for sensory-evoked LTP that is independent of somatic spikes, displaying similarities to
in vitro
experiments in the hippocampus.
Long-term synaptic potentiation (LTP) is thought to be a key process in cortical synaptic network plasticity and memory formation
1
. Hebbian forms of LTP depend on strong postsynaptic depolarization, which in many models is generated by action potentials that propagate back from the soma into dendrites
2
,
3
. However, local dendritic depolarization has been shown to mediate these forms of LTP as well
1
,
4
,
5
. As pyramidal cells in supragranular layers of the somatosensory cortex spike infrequently
6
,
7
,
8
, it is unclear which of the two mechanisms prevails for those cells
in vivo
. Using whole-cell recordings in the mouse somatosensory cortex
in vivo
, we demonstrate that rhythmic sensory whisker stimulation efficiently induces synaptic LTP in layer 2/3 (L2/3) pyramidal cells in the absence of somatic spikes. The induction of LTP depended on the occurrence of NMDAR (
N
-methyl-
d
-aspartate receptor)-mediated long-lasting depolarizations, which bear similarities to dendritic plateau potentials
9
,
10
,
11
,
12
,
13
. In addition, we show that whisker stimuli recruit synaptic networks that originate from the posteromedial complex of the thalamus (POm). Photostimulation of channelrhodopsin-2 expressing POm neurons generated NMDAR-mediated plateau potentials, whereas the inhibition of POm activity during rhythmic whisker stimulation suppressed the generation of those potentials and prevented whisker-evoked LTP. Taken together, our data provide evidence for sensory-driven synaptic LTP
in vivo
, in the absence of somatic spiking. Instead, LTP is mediated by plateau potentials that are generated through the cooperative activity of lemniscal and paralemniscal synaptic circuitry
14
,
15
,
16
.