Sensory races between motor control brain areas for coordinating how to react to the outside world

• Applicant: Professor Ziad Hafed, Ph.D., since 4/2022
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: since 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 457750211

Interacting with the surrounding environment requires a fine balance between following internal goals while maintaining sensitivity to external events. Since the 1980’s, the main perspective in cognitive neuroscience has been to study how the brain selects the appropriate behavior in reaction to an external event. Thus, the primary experimental approach was to rely on highly well controlled “trials” in which specific sensory task events occur and specific behavioral outputs are measured. However, no matter how well controlled intra-trial experimental events are, the trials themselves and their first sensory stimuli necessarily come asynchronously to the ongoing internal brain state. This creates what we call a “race condition” between the processing of the new external information and the completion of internal plans. In the present proposal, we will study this race condition in the visual modality and with eye movements. We argue that before any orienting eye movement response to the outside world can happen, an interruption of internal ongoing processes must first take place. We will rigorously investigate the neurophysiological basis underpinning a very early and automatic interrupt process caused by exogenous events. Our primary hypothesis is that endowing neurons at the edge of the motor control periphery with early visual sensitivity might help in handling the coordination needed between whether to orient to the outside stimulus or whether to first complete execution of an already planned movement. To that end, we will study omnipause neurons (OPNs) located in the brainstem, which gate eye movements by maintaining inhibition upon saccade burst neurons and only allow saccades when they pause. We will show that OPNs, in fact, exhibit a vast and intriguing repertoire of visual responses. Their inhibitory properties, together with their visual sensitivity, make them the perfect candidate to support interruption of ongoing oculomotor behavior before responding to exogenous stimuli. On the other hand, sensory properties in a neighboring structure, superior colliculus (SC), support orienting behaviour instead. Understanding how a sensory race between OPNs and SC underlies flexible motor behavior will provide a highly mechanistic description of exactly what to expect in terms of the final motor response when external stimuli come asynchronously to internal brain state. The transformative aspect of the proposal is that it will strongly recast traditional interpretations of the functional roles of late motor control structures in the lower brainstem. Moreover, the concept of interruption explored in the proposal can clarify a wide variety of neurophysiological observations related not only to oculomotor control circuitry, but also to cognitive and perceptual processes, providing deeper explanation of some of the most classic cognitive findings in the attention literature, as well as findings related to decision processes underlying overt orienting.

• DFG Programme: Research Grants
• Ehemaliger Antragsteller: Antimo Buonocore, Ph.D., until 3/2022