Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision

TY - JOUR

T1 - Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision

AU - Schaefer, Andreas T

AU - Angelo, Kamilla

AU - Spors, Hartwig

AU - Margrie, Troy W

N1 - Keywords: Action Potentials; Animals; Electrophysiology; Evoked Potentials; Female; Male; Mice; Neurons; Olfactory Bulb; Pattern Recognition, Physiological

PY - 2006

Y1 - 2006

N2 - Although oscillations in membrane potential are a prominent feature of sensory, motor, and cognitive function, their precise role in signal processing remains elusive. Here we show, using a combination of in vivo, in vitro, and theoretical approaches, that both synaptically and intrinsically generated membrane potential oscillations dramatically improve action potential (AP) precision by removing the membrane potential variance associated with jitter-accumulating trains of APs. This increased AP precision occurred irrespective of cell type and--at oscillation frequencies ranging from 3 to 65 Hz--permitted accurate discernment of up to 1,000 different stimuli. At low oscillation frequencies, stimulus discrimination showed a clear phase dependence whereby inputs arriving during the trough and the early rising phase of an oscillation cycle were most robustly discriminated. Thus, by ensuring AP precision, membrane potential oscillations dramatically enhance the discriminatory capabilities of individual neurons and networks of cells and provide one attractive explanation for their abundance in neurophysiological systems.

AB - Although oscillations in membrane potential are a prominent feature of sensory, motor, and cognitive function, their precise role in signal processing remains elusive. Here we show, using a combination of in vivo, in vitro, and theoretical approaches, that both synaptically and intrinsically generated membrane potential oscillations dramatically improve action potential (AP) precision by removing the membrane potential variance associated with jitter-accumulating trains of APs. This increased AP precision occurred irrespective of cell type and--at oscillation frequencies ranging from 3 to 65 Hz--permitted accurate discernment of up to 1,000 different stimuli. At low oscillation frequencies, stimulus discrimination showed a clear phase dependence whereby inputs arriving during the trough and the early rising phase of an oscillation cycle were most robustly discriminated. Thus, by ensuring AP precision, membrane potential oscillations dramatically enhance the discriminatory capabilities of individual neurons and networks of cells and provide one attractive explanation for their abundance in neurophysiological systems.

U2 - 10.1371/journal.pbio.0040163

DO - 10.1371/journal.pbio.0040163

M3 - Journal article

C2 - 16689623

SN - 1544-9173

VL - 4

SP - e163

JO - PLoS Biology

JF - PLoS Biology

IS - 6

ER -