Intracortical Microstimulation Modulates Cortical Induced Responses

Recent advances in cortical prosthetics relied on intracortical microstimulation (ICMS) to activate the cortical neural network and convey information to the brain. Here we show that activity elicited by low-current ICMS modulates induced cortical responses to a sensory stimulus in the primary auditory cortex (A1). A1 processes sensory stimuli in a stereotyped manner, encompassing two types of activity: evoked activity (phase-locked to the stimulus) and induced activity (non-phase-locked to the stimulus). Time-frequency analyses of extracellular potentials recorded from all layers and the surface of the auditory cortex of anesthetized guinea pigs of both sexes showed that ICMS during the processing of a transient acoustic stimulus differentially affected the evoked and induced response. Specifically, ICMS enhanced the long-latency-induced component, mimicking physiological gain increasing top-down feedback processes. Furthermore, the phase of the local field potential at the time of stimulation was predictive of the response amplitude for acoustic stimulation, ICMS, as well as combined acoustic and electric stimulation. Together, this was interpreted as a sign that the response to electrical stimulation was integrated into the ongoing cortical processes in contrast to substituting them. Consequently, ICMS modulated the cortical response to a sensory stimulus. We propose such targeted modulation of cortical activity (as opposed to a stimulation that substitutes the ongoing processes) as an alternative approach for cortical prostheses.

SIGNIFICANCE STATEMENT Intracortical microstimulation (ICMS) is commonly used to activate a specific subset of cortical neurons, without taking into account the ongoing activity at the time of stimulation. Here, we found that a low-current ICMS pulse modulated the way the auditory cortex processed a peripheral stimulus, by supra-additively combining the response to the ICMS with the cortical processing of the peripheral stimulus. This artificial modulation mimicked natural modulations of response magnitude such as attention or expectation. In contrast to what was implied in earlier studies, this shows that the response to electrical stimulation is not substituting ongoing cortical activity but is integrated into the natural processes.

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