Studying induced and evoked oscillations for probing visual and auditory circuit mechanisms

Abstract

Specialized sensory regions process incoming sensory inputs using a variety of mechanisms, such as normalization and excitatory-inhibitory interactions. These mechanisms can be studied through induced and evoked oscillations, which serve as measurable read-outs. In this work, we empirically studied these oscillations to understand the circuit properties and whether those are preserved across visual and auditory modalities.

One of the indicators of excitatory-inhibitory interactions are narrow-band gamma (30-70 Hz) oscillations, which can be induced by presenting certain visual stimuli. These stimulus-induced oscillations weaken with healthy aging and at the onset of Alzheimer’s disease and hence hold promise as a potential biomarker. However, delivering visual stimuli is cumbersome, as it requires head stabilization for eye tracking; an equivalent auditory paradigm could be helpful. We tested whether auditory ripple stimuli, an analogue to visual gratings, could elicit narrow-band oscillations in auditory areas. For our first study, we recorded a 64-channel EEG from subjects who either fixated on the monitor while passively viewing static visual gratings, or listened to stationary and moving ripples, played using loudspeakers, with their eyes open or closed. We found that while visual gratings induced narrow-band gamma oscillations with suppression in the alpha band, auditory ripples did not produce narrow-band gamma but instead elicited robust broadband high-gamma (70-150 Hz) response and suppression in the beta band. So, even though we used equivalent stimuli in both modalities, our findings indicate that the underlying neuronal circuitry may not share ubiquitous strategies for generating induced oscillations. To further elucidate whether the broadband activity obtained in response to the ripple stimuli is not simply multiple narrow-band gamma oscillations at different bands and to check the selectivity of broadband gamma towards stimulus features, we recorded ECoG activity from the exposed auditory cortex of patients with refractory epilepsy. We observed that ripple stimuli induce broadband gamma activity, which is stimulus-selective for slowly modulating ripple stimuli.

Studies focusing on attention and brain-computer interfaces often use multiple temporally modulated stimuli simultaneously, which involves gain modulation through a process called normalization. Such stimuli produce a time-locked oscillatory response called the steady-state visual evoked response (SSVEP) or the auditory steady-state response (ASSR) in visual and auditory modalities. Presentation of multiple stimuli together leads to suppression of the steady-state response. We investigated if the amount of suppression changes as a function of the frequency of competing stimuli and the dynamics of the normalization model. For our second study, we presented two overlapping counterphasing grating stimuli (plaids), either parallelly or orthogonally, at multiple contrasts and temporal frequencies, and recorded spikes, local field potential, and electrocorticogram activity from macaque primary visual cortex (V1) while they passively fixated. The resulting SSVEPs exhibited complicated dynamics – with “low-pass” and “band-pass” suppression profiles for orthogonal and parallel plaids, respectively. Surprisingly, adding a simple low-pass filter to the normalization signal sufficiently explained these diverse effects. In our third study, we studied the same in the auditory modality. We played sinusoidally amplitude-modulated stimuli simultaneously modulated at two frequencies while recording 64-channel EEG from subjects who passively listened to these sounds with closed eyes. We obtained a band-pass shaped suppression profile for ASSRs with a low-pass cutoff similar to that observed for SSVEP interactions, and the same slow-varying normalization model could capture this. Our findings highlight the canonical nature of the normalization model in accounting for interactions among evoked oscillations.