Cortical Membrane Potential Signature of Optimal States for Sensory Signal Detection

The neural correlates of optimal states for signal detection task performance are largely unknown. One hypothesis holds that optimal states exhibit tonically depolarized cortical neurons with enhanced spiking activity, such as occur during movement. We recorded membrane potentials of auditory cortic...

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Bibliographic Details
Published in:	Neuron (Cambridge, Mass.) Mass.), 2015-07, Vol.87 (1), p.179-192
Main Authors:	McGinley, Matthew J., David, Stephen V., McCormick, David A.
Format:	Article
Language:	eng
Subjects:	Animals Arousal - physiology Auditory Cortex - cytology Auditory Cortex - physiology Auditory Perception - physiology Behavior Confidence intervals Membrane Potentials - physiology Mice Neurons Neurons - physiology Physiology Signal Detection, Psychological - physiology Studies
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Summary:	The neural correlates of optimal states for signal detection task performance are largely unknown. One hypothesis holds that optimal states exhibit tonically depolarized cortical neurons with enhanced spiking activity, such as occur during movement. We recorded membrane potentials of auditory cortical neurons in mice trained on a challenging tone-in-noise detection task while assessing arousal with simultaneous pupillometry and hippocampal recordings. Arousal measures accurately predicted multiple modes of membrane potential activity, including rhythmic slow oscillations at low arousal, stable hyperpolarization at intermediate arousal, and depolarization during phasic or tonic periods of hyper-arousal. Walking always occurred during hyper-arousal. Optimal signal detection behavior and sound-evoked responses, at both sub-threshold and spiking levels, occurred at intermediate arousal when pre-decision membrane potentials were stably hyperpolarized. These results reveal a cortical physiological signature of the classically observed inverted-U relationship between task performance and arousal and that optimal detection exhibits enhanced sensory-evoked responses and reduced background synaptic activity. [Display omitted] •Optimal performance of mice on an auditory detection task occurs at moderate arousal•Large, reliable sub- and supra-threshold sensory responses occur at moderate arousal•Hyperpolarized, quiescent membrane potentials precede correct detection events•Pupil diameter predicts cortical dynamic states governing detection task performance McGinley et al. reveal the cortical membrane potential dynamics underlying the classically-observed inverted-U dependence of detection task performance on arousal (measured using pupillometry). Optimal arousal exhibits large, reliable sensory-evoked spiking and postsynaptic potentials responses and hyperpolarized, quiescent background membrane potentials.
ISSN:	0896-6273 1097-4199