Journal Article

Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice

Petersen, Carl C. H., Poulet, James F. A.

2008

Overview

Neurocomputation: degrees of cortical processing Differences in synchronized activity in cortical neurons characterize different brain states, and are thought to be fundamental mechanisms of neural computation. James Poulet and Carl Petersen now show using dual whole-cell recordings from somatosensory barrel cortex in behaving mice, that the membrane potential of nearby neurons is highly correlated during quiet wakefulness but this correlation is reduced when the mice were actively whisking — a stereotypic back-and-forth movement of the whickers used to explore the environment. This suggests that internal brain states dynamically regulate cortical membrane potential synchrony during behaviour, defining different modes of cortical processing. Differences in synchronized activity in cortical neurons characterize different brain states. Petersen and colleagues now show that in mice the membrane potential of nearby neurons is highly correlated during quiet wakefulness but this correlation is reduced when mice are actively whisking. This suggests that internal brain states dynamically regulate cortical membrane potential synchrony during behaviour. Internal brain states form key determinants for sensory perception, sensorimotor coordination and learning 1 , 2 . A prominent reflection of different brain states in the mammalian central nervous system is the presence of distinct patterns of cortical synchrony, as revealed by extracellular recordings of the electroencephalogram, local field potential and action potentials. Such temporal correlations of cortical activity are thought to be fundamental mechanisms of neuronal computation 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 . However, it is unknown how cortical synchrony is reflected in the intracellular membrane potential ( V m ) dynamics of behaving animals. Here we show, using dual whole-cell recordings from layer 2/3 primary somatosensory barrel cortex in behaving mice, that the V m of nearby neurons is highly correlated during quiet wakefulness. However, when the mouse is whisking, an internally generated state change reduces the V m correlation, resulting in a desynchronized local field potential and electroencephalogram. Action potential activity was sparse during both quiet wakefulness and active whisking. Single action potentials were driven by a large, brief and specific excitatory input that was not present in the V m of neighbouring cells. Action potential initiation occurs with a higher signal-to-noise ratio during active whisking than during quiet periods. Therefore, we show that an internal brain state dynamically regulates cortical membrane potential synchrony during behaviour and defines different modes of cortical processing.

• Publisher: Nature Publishing Group UK,Nature Publishing,Nature Publishing Group
• Subject: Animal behavior / Animal models in research / Animals / Biological and medical sciences / Brain / Brain research / Cellular biology / Central nervous system / Electroencephalography / Exploratory Behavior - physiology / Fundamental and applied biological sciences. Psychology / Humanities and Social Sciences / letter / Male / Membrane potentials / Membrane Potentials - physiology / Membranes / Mice / Mice, Inbred C57BL / multidisciplinary / Neurology / Neurons - physiology / Physiological aspects / Rodents / Science / Science (multidisciplinary) / Sleep. Vigilance / Somatosensory Cortex - physiology / Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors / State regulations / Vertebrates: nervous system and sense organs / Wakefulness - physiology