Causally Investigating Cortical Dynamics and Signal Processing by Targeting Natural System Attractors With Precisely Timed (Electrical) Stimulation

Abstract

Electrical stimulation is a promising tool for interacting with neuronal dynamics to identify neural mechanisms that underlie cognitive function. Since effects of a single short stimulation pulse typically vary greatly and depend on the current network state, many experimental paradigms have rather resorted to continuous or periodic stimulation in order to establish and maintain a desired effect. However, such an approach explicitly leads to forced and “unnatural” brain activity. Further, continuous stimulation can make it hard to parse the recorded activity and separate neural signal from stimulation artifacts. In this study we propose an alternate strategy: by monitoring a system in realtime, we use the existing preferred states or attractors of the network and apply short and precise pulses in order to switch between those states. When pushed into one of its attractors, one can use the natural tendency of the system to remain in such a state to prolong the effect of a stimulation pulse, opening a larger window of opportunity to observe the consequences on cognitive processing. To elaborate on this idea, we consider flexible information routing in the visual cortex as a prototypical example. When processing a stimulus, neural populations in the visual cortex have been found to engage in synchronized gamma activity. In this context, selective signal routing is achieved by changing the relative phase between oscillatory activity in sending and receiving populations (communication through coherence, CTC). In order to explore how perturbations interact with CTC, we investigate a network of interneuronal gamma (ING) oscillators composed of integrate-and-fire neurons exhibiting similar synchronization and signal routing phenomena. We develop a closed-loop stimulation paradigm based on the phase-response characteristics of the network and demonstrate its ability to establish desired synchronization states. By measuring information content throughout the model, we evaluate the effect of signal contamination caused by the stimulation in relation to the magnitude of the injected pulses and intrinsic noise in the system. Finally, we demonstrate that, up to a critical noise level, precisely timed perturbations can be used to artificially induce the effect of attention by selectively routing visual signals to higher cortical areas.

Neurostimulation and Therapeutic Advance: Iterative or Principled?

“…For neurostimulation precise temporal and spatial resolution constitutes an ideal objective, with limited interrogation intervention. However, due to the dynamic nature of the oscillator field the effects of carefully circumscribed stimuli can be shortlived [24]. Critically, as noted, such impact is highly dependent on the state of the field.…”

Dynamical Phase Modulation and Oscillatory Detuning in Applied Neurostimulation

“…Noise, particularly, is intrinsic to neural activity, and can be expected to exacerbate the degradation of partial phase locking occurring between oscillators during detuning intervals (or neural networks approximated by oscillators) [19]. There is, for example, indirect evidence that for cortical gamma oscillations the frequency and amplitude evolution over time is noisy and complex [40] and changes as a function of cortical state [41].…”

“…For neurostimulation precise temporal and spatial resolution constitutes an ideal objective, with minimal interrogation of target oscillators. However, due to the dynamic nature of the oscillator field the effects of carefully circumscribed stimuli can be short-lived [19]. Critically, such impact is highly dependent on the state of the neural field.…”