Visuomotor temporal adaptation is tuned to gamma brain oscillatory coherence

ABSTRACTEvery time we use our smartphone, tablet, or other electronic devices we are exposed to temporal delays between our actions and the sensory feedback. We can compensate for such delays by adjusting our motor commands and doing so likely requires establishing new temporal mappings between motor areas and sensory predictions. However, little is known about the neural underpinnings that would support building new temporal correspondences between different brain areas. We here address the possibility that communication through coherence, which is thought to support neural interareal communication, lies behind the neural processes accounting for how humans cope with additional delays between motor and sensory areas. We recorded EEG activity while participants intercepted moving targets while seeing a cursor that followed their hand with a delay rather than their own hand. Participants adjusted their movements to the delayed visual feedback and intercepted the target with the cursor. The EEG data shows a significant increase in coherence of beta and gamma bands between visual and motor areas during the hand on-going movement towards interception. However, when looking at differences between participants depending on the level of adaptation, only the increase in gamma band correlated with the level of temporal adaptation. We are able to describe the time course of the coherence using coupled oscillators showing that the times at which high coherence is achieved are within useful ranges to solve the task. Altogether, these results evidence the functional relevance of brain coherence in a complex task where adapting to new delays is crucial.AUTHOR SUMMARYHumans are often exposed to delays between their actions and the incoming sensory feedback caused by actions. While there have been advances in the understanding of the conditions at which temporal adaptation can occur, little is known about the neural mechanisms enabling temporal adaptation. In the present study we measure brain activity (EEG) to investigate whether communication through coherence between motor and sensory areas might be responsible for one’s ability to cope with externally imposed delays in an interception task. We show evidence that neural coherence at gamma band between visual and motor areas is related to the degree of adaptation to temporal delays.

Communication through coherence by means of cross-frequency coupling

The theory of communication through coherence (CTC) posits the synchronization of brain oscillations as a key mechanism for information sharing and perceptual binding. In a parallel literature, hippocampal theta activity (4 – 10 Hz) has been shown to modulate the appearance of neocortical fast gamma oscillations (100 – 150 Hz), a phenomenon known as cross-frequency coupling (CFC). Even though CFC has also been previously associated with information routing, it remains to be determined whether it directly relates to CTC. In particular, for the theta-fast gamma example at hand, a critical question is to know if the phase of the theta cycle influences gamma synchronization across the neocortex. To answer this question, we designed a new screening method for detecting the modulation of the cross-regional high-frequency synchronization by the phase of slower oscillations. Upon applying the method, we found that the long-distance synchronization of neocortical fast gamma during REM sleep depends on the instantaneous phase of the theta rhythm. These results show that CFC is likely to aid long-range information transfer by facilitating the cross-regional synchronization of faster rhythms, thus consistent with classical CTC views.

Brain State-dependent Gain Modulation of Corticospinal Output in the Active Motor System

The communication through coherence hypothesis suggests that only coherently oscillating neuronal groups can interact effectively and predicts an intrinsic response modulation along the oscillatory rhythm. For the motor cortex (MC) at rest, the oscillatory cycle has been shown to determine the brain’s responsiveness to external stimuli. For the active MC, however, the demonstration of such a phase-specific modulation of corticospinal excitability (CSE) along the rhythm cycle is still missing. Motor evoked potentials in response to transcranial magnetic stimulation (TMS) over the MC were used to probe the effect of cortical oscillations on CSE during several motor conditions. A brain–machine interface (BMI) with a robotic hand orthosis allowed investigating effects of cortical activity on CSE without the confounding effects of voluntary muscle activation. Only this BMI approach (and not active or passive hand opening alone) revealed a frequency- and phase-specific cortical modulation of CSE by sensorimotor beta-band activity that peaked once per oscillatory cycle and was independent of muscle activity. The active MC follows an intrinsic response modulation in accordance with the communication through coherence hypothesis. Furthermore, the BMI approach may facilitate and strengthen effective corticospinal communication in a therapeutic context, for example, when voluntary hand opening is no longer possible after stroke.

Gamma synchronization between V1 and V4 improves behavioral performance

ABSTRACTMotor behavior is often driven by visual stimuli, relying on efficient feedforward communication from lower to higher visual areas. The Communication-through-Coherence hypothesis proposes that interareal communication depends on coherence at an optimal phase relation. While previous studies have linked effective communication to enhanced interareal coherence, it remains unclear, whether this interareal coherence occurs at an optimal phase relation that actually improves the stimulus transmission to behavioral report. We recorded local field potentials simultaneously from areas V1 and V4 of macaque monkeys performing a selective visual attention task, during which they reported changes of the attended stimulus. Gamma synchronization between V1 and V4, immediately preceding the stimulus change, predicted subsequent reaction times (RTs). Crucially, RTs were systematically slowed as trial-by-trial interareal gamma phase relations deviated from the phase relation at which V1 and V4 synchronized on average. These effects were specific to the attended stimulus and not due to local power or phase inside V1 or V4. We conclude that interareal gamma synchronization occurs at the optimal phase relation and thereby improves interareal communication and the effective transformation of sensory inputs into motor responses.

Selective Interareal Synchronization through Gamma Frequency Differences and Slower-Rhythm Gamma Phase Reset

The communication-through-coherence (CTC) hypothesis states that a sending group of neurons will have a particularly strong effect on a receiving group if both groups oscillate in a phase-locked (“coherent”) manner (Fries, 2005 , 2015 ). Here, we consider a situation with two visual stimuli, one in the focus of attention and the other distracting, resulting in two sites of excitation at an early cortical area that project to a common site in a next area. Taking a modeler’s perspective, we confirm the workings of a mechanism that was proposed by Bosman et al. ( 2012 ) in the context of providing experimental evidence for the CTC hypothesis: a slightly higher gamma frequency of the attended sending site compared to the distracting site may cause selective interareal synchronization with the receiving site if combined with a slow-rhythm gamma phase reset. We also demonstrate the relevance of a slightly lower intrinsic frequency of the receiving site for this scenario. Moreover, we discuss conditions for a transition from bottom-up to top-down driven phase locking.