Selective neuronal lapses precede human cognitive lapses following sleep deprivation

Abstract

Sleep deprivation (SD) is a major source of morbidity with widespread health effects including increased risks of hypertension, diabetes, obesity, heart attack, and stroke ¹ . Moreover, SD brings about vehicle accidents and medical errors ^{2– 4} , and is therefore an urgent topic of investigation. During SD, homeostatic and circadian processes interact to build up sleep pressure ⁵ that results in slow behavioral performance (cognitive lapses) typically attributed to attentional thalamic and fronto-parietal circuits ^{6– 14} , but the underlying mechanisms remain unclear ^{3, 15} . Recently, it was found in human electroencephalogram (EEG) ^{16, 17} and in the local field potential (LFP) of non-human primates ¹⁸ and rodents ¹⁹ that during SD, regional ‘sleep-like’ slow/theta waves co-occur with impaired behavioral performance during wakefulness. Here we used intracranial electrodes to record single-neuron and LFP activities in human neurosurgical patients performing a face/non-face categorization psychomotor vigilance task (PVT) ^{20– 24} in multiple experimental sessions, including after full-night SD. We find that just before cognitive lapses, selective spiking responses of individual neurons in the medial temporal lobe (MTL) are attenuated, delayed, and lengthened. These ‘neuronal lapses’ are evident on a trial-by-trial basis comparing the slowest behavioral PVT reaction times to the fastest. Furthermore, during cognitive lapses LFPs exhibit a relative local increase in slow/theta activity that is correlated with degraded single-neuron responses and with baseline theta activity. Our results show that cognitive lapses involve local state-dependent changes in neuronal activity already in the MTL.