Response adaptation in barrel cortical neurons facilitates stimulus detection during rhythmic whisker stimulation in anesthetized mice

Abstract

Rodents use rhythmic whisker movements at frequencies between 4-12 Hz to sense the environment that will be disturbed when the animal touches an object. The aim of this work is to study the response adaptation to rhythmic whisker stimulation trains at 4 Hz in the barrel cortex and the sensitivity of cortical neurons to changes in the timing of the stimulation pattern. Longitudinal arrays of four Iridium oxide electrodes were used to obtain single-unit recordings in supra-, granular and infragranular neurons in urethane anesthetized mice. The stimulation protocol consisted in a stimulation train of 3 air-puffs (20 ms duration each) in which the time interval between the first and the third stimuli was fixed (500 ms) and the time interval between the first and the second stimuli changed (regular: 250 ms; “accelerando”: 375 ms; or “decelerando” stimulation train: 125 ms interval). Cortical neurons adapted strongly their response to regular stimulation trains. Response adaptation was reduced when “accelerando” or “decelerando” stimulation trains were applied. This facilitation of the shifted stimulus was mediated by activation of NMDA receptors since the effect was blocked by AP5. The facilitation was not observed in thalamic nuclei. Facilitation increased during periods of EEG activation induced by systemic application of IGF-I, probably by activation of NMDA receptors, as well. We suggest that response adaptation is the outcome of an intrinsic cortical information processing aimed at contributing to improve the detection of “unexpected” stimuli that disturbed the rhythmic behavior of exploration.

Significance Statement To detect objects, rodents scan the environment by rhythmic movements of whiskers at 4-12 Hz, suggesting that this rhythmic behavior may facilitate stimulus detection. This rhythmic input in the somatosensory cortex will be disturbed when the animal touches an object. We study if spike responses in the somatosensory cortex are sensitive to small changes in the timing of the rhythmic sensory input. We find that responses were facilitated when a modification of the stimulation interval was introduced in the stimulation sequence. This facilitation was mediated by activation of NMDA receptors and increased during periods of EEG activation induced by IGF-I application. We suggest that the detection mechanism of shifted stimulus may play a role in sensory processing.