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Boosting Reward-based Attention through VEstibular STimulation

Periodic Reporting for period 1 - BRAVEST (Boosting Reward-based Attention through VEstibular STimulation)

Periodo di rendicontazione: 2018-02-01 al 2020-01-31

Intrinsically rewarding stimuli can strongly capture human spatial attention. This phenomenon contributes in creating some abstract “priority map” of the surrounding environment, which is therefore explored and exploited more effectively. Neuroimaging studies suggest that the Anterior Cingulate Cortex (ACC) holds an important role in orienting attention in space as a function of the perceived value of external stimuli. The ACC is located deep beneath the brain’s surface, and therefore it is hardly reachable with common neurostimulation devices. In contrast, Galvanic Vestibular Stimulation (GVS) has been consistently shown to activate deep brain structures involved in mood and affective processing. GVS is a safe way to stimulate the vestibular system through weak electric currents applied behind the ears; the activity of the VIII cranial nerve is modulated, resulting in mild illusions of self-movement.
The first objective of the action was studying whether GVS is capable to affect human motivation, in light of these subcortical brain activations. Specifically, we sought to assess whether spatial attention is oriented by rewards, during GVS, differently with respect to sham stimulation.
We reasoned that this could have clinical implications. Often, after stroke, patients may present difficulties in orienting attention toward the region of space opposite to the brain lesion (Unilateral Spatial Neglect, USN). USN has a strong and debilitating impact on daily life activities. Should GVS promote attentional orienting by value information, this technique could be used in combination with ad hoc behavioral paradigms aimed at maximizing the exploration of the neglected side of space. Testing this possibility was the second objective of the proposal.
We administered GVS (or sham stimulation) to healthy individuals engaged in an attentional task. The attentional task (AT) was a spatial cueing paradigm: lateralized targets were presented following a cue which could appear on the same side of the screen (congruent condition) or on the opposite side (incongruent condition). Behavioral differences between congruent and incongruent conditions provide indications about the distribution of spatial attention. Furthermore, the cue could also inform participants about the amount of (monetary) reward at stake. Thus, the AT was designed to measure: 1) performance improvements for cues signaling high rewards; 2) the differential distribution of attention as a function of the value at stake. We have found no evidence for GVS to affect how attention is distributed in space according to the value at stake. However, we have found that GVS reduces sensitivity to rewards. Overall, high rewards at stake boosted participants’ performance; however, this effect was reduced while they were receiving GVS. Results are described in Blini, Tilikete, Farné, and Hadj-Bouziane, (2018, Cortex).
Results have been discussed as originating from visuo-vestibular mismatches, a fundamental, yet overlooked, bodily signal. Visual and vestibular information are usually tightly linked, hence their uncoupling raises several flags. For example, visuo-vestibular mismatches can be subtle, but informative, warning signals which follow the ingestion of noxious neurotoxins, hence the association with nausea, disgust, and vomiting (an attempt to expel them), and the proposed role in aversive conditioning. Thus, results echoed an embodied mechanism to evaluate the desirability of rewards, which seems to extend to secondary-abstract ones (i.e. monetary rewards), and may largely depend on interoception, namely the ability to perceive our innermost physiological states.
With this new evidence, we decided to amend our second objective. As GVS does not affect the interplay between attention and motivation, and additionally reduces performance improvements associated to rewards, we worried that patients with USN would not gain additional benefit from this technique. Instead, we reasoned that GVS may benefit clinical populations in which sensitivity to rewards is extreme, e.g. Addiction Disorders (AD). We have thus designed a task supposedly closer to the clinical picture of AD patients. Specifically, we designed a task capable to measure both motivation and executive functions, i.e. the ability to inhibit irrelevant and conflicting information. In addition, we evaluated the impact of GVS on negative reinforcers (i.e. monetary losses). We have found, indeed, evidence for GVS to increase sensitivity to losses, causing overall increased distraction when losses are at stake. These results suggest that, when the value of one stimulus must be computed, the information arising from bodily processes is taken into account. GVS, through a perturbation of the vestibular system, may bias the desirability of stimuli toward a more negative valence attribution. Positive reinforcers would be, in the context of visuo-vestibular mismatches, devalued; negative ones – whose intrinsic valence matches the current physiological state, meant to arise in perturbed physiological states, e.g. motion sickness – would instead gain in salience. In summary, interoceptive signals drive human motivation, and GVS may be a useful tool to probe this link experimentally. Results are described in a pre-print (Blini, Tilikete, Chelazzi, Farné, and Hadj-Bouziane, submitted,
During the course of this action, we strived to adhere to the golden standards of Open Science. Results have been published with the Open Access formula, and are thus public. Raw data, materials, and annotated scripts are public as well. The studies have been pre-registered and preliminarily submitted for publication as registered reports. This new format enables full transparency of the experimental protocol and pipeline, enhancing the credibility of reported findings and mitigating publication bias (as findings are published regardless of the final results). Dissemination has been performed through social media (e.g. Kudos, ResearchGate, Twitter, Facebook, Linkedin) and traditional venues; all the materials are publicly available as well ( Outreach to a broader audience occurred on social media (e.g. Twitter, Facebook), through individual debriefing for participants to the studies, ad hoc events (e.g. la fête de la science – researchers’ night France, the Web Conf), or initiatives promoted by the Lyon Neuroscience Center (such as Open days for high-school students).
There is growing interest around the somatic determinants of human decision-making. Here we show that a vestibular perturbation, and visuo-vestibular mismatches, may represent an important interoceptive signal guiding motivated behavior. Research on interoception has been so far skewed toward respiratory, cardiac, or gastric signals, but here we have provided evidence for including visuo-vestibular mismatches between these important bodily signals, as well as a safe and convenient method (GVS) for experimental manipulations. A safe technique capable of decreasing sensitivity to reward may inform greatly cognitive models of motivation, but also help the management of clinical populations for which an extreme sensitivity to short-term rewards has been described.