A Cortical Mechanism Linking Saliency Detection and Motor Reactivity in Rhesus Monkeys.

Sudden and surprising sensory events trigger neural processes that swiftly adjust behavior. To study the phylogenesis and the mechanism of this phenomenon, we trained two male rhesus monkeys to keep a cursor inside a visual target by exerting force on an isometric joystick. We examined the effect of surprising auditory stimuli on exerted force, scalp electroencephalographic (EEG) activity, and local field potentials (LFPs) recorded from the dorsolateral prefrontal cortex. Auditory stimuli elicited (1) a biphasic modulation of isometric force, a transient decrease followed by a corrective tonic increase, and (2) EEG and LFP deflections dominated by two large negative-positive waves (N70 and P130). The EEG potential was symmetrical and maximal at the scalp vertex, highly reminiscent of the human "vertex potential." Electrocortical potentials and force were tightly coupled: the P130 amplitude predicted the magnitude of the corrective force increase, particularly in the LFPs recorded from deep rather than superficial cortical layers. These results disclose a phylogenetically preserved corticomotor mechanism supporting adaptive behavior in response to salient sensory events.Significance Statement Survival in the natural world depends on an animal's capacity to adapt ongoing behavior to abrupt unexpected events. To study the neural mechanisms underlying this capacity, we trained monkeys to apply constant force on a joystick while we recorded their brain activity from the scalp and the prefrontal cortex contralateral to the hand holding the joystick. Unexpected auditory stimuli elicited a biphasic force modulation: a transient reduction followed by a corrective adjustment. The same stimuli also elicited EEG and LFP responses, dominated by a biphasic wave that predicted the magnitude of the behavioral adjustment. These results disclose a phylogenetically preserved corticomotor mechanism supporting adaptive behavior in response to unexpected events.

Spatial uncertainty improves the distribution of visual attention and the availability of sensory information for conscious report.

Picking-up and exploiting spatial and temporal regularities in the occurrence of sensory events is important for goal-directed behaviour. According to the "Predictive Coding Hypothesis" (Friston Philosophical Trans R Soc B 360(1456):815-836, 2005), these regularities are used to generate top-down predictions that are constantly compared with actual sensory events. In a previous study with the Attentional Blink (AB) paradigm, we showed that the temporal and probabilistic uncertainty of T2s that are presented outside the Attentional Blink period, i.e. at least 400 ms after T1, improves the conscious report of T2 that are presented inside the AB. The study of ERP correlated showed that this improvement was associated with a prolonged storage of pre-conscious T2 traces in extra-striate areas (Lasaponara et al. Cortex 71:15-33, 2015). Here, we tested whether variations in the probabilistic cueing of the position of a primary T1 visual target in a 4 × 4 letter array, modulate the retention of memory traces evoked by secondary letter targets (T2) that were presented in other positions of the array. Most important, in each trial, the identity of T2 was specified to participants upon disappearance of the array. We show that high probabilistic cueing facilitates T1 detection and improves the corresponding sensitivity index (d'). In contrast, retention and conscious report of secondary targets (T2) improves when the probabilistic cueing of T1 position is poor. These results suggest that uncertainty in the upcoming position of primary targets boosts the strength of memory traces evoked by secondary targets and improves the possibility that traces of secondary targets gain full access to conscious processing.

Deconstructing Reorienting of Attention: Cue Predictiveness Modulates the Inhibition of the No-target Side and the Hemispheric Distribution of the P1 Response to Invalid Targets.

Orienting of attention produces a "sensory gain" in the processing of visual targets at attended locations and an increase in the amplitude of target-related P1 and N1 ERPs. P1 marks gain reduction at unattended locations; N1 marks gain enhancement at attended ones. Lateral targets that are preceded by valid cues also evoke a larger P1 over the hemisphere contralateral to the no-target side, which reflects inhibition of this side of space [Slagter, H. A., Prinssen, S., Reteig, L. C., & Mazaheri, A. Facilitation and inhibition in attention: Functional dissociation of pre-stimulus alpha activity, P1, and N1 components. Neuroimage, 125, 25-35, 2016]. To clarify the relationships among cue predictiveness, sensory gain, and the inhibitory P1 response, we compared cue- and target-related ERPs among valid, neutral, and invalid trials with predictive (80% valid/20% invalid) or nonpredictive (50% valid/50% invalid) directional cues. Preparatory facilitation over the visual cortex contralateral to the cued side of space (lateral directing attention positivity component) was reduced during nonpredictive cueing. With predictive cues, the target-related inhibitory P1 was larger over the hemisphere contralateral to the no-target side not only in response to valid but also in response to neutral and invalid targets: This result highlights a default inhibitory hemispheric asymmetry that is independent from cued orienting of attention. With nonpredictive cues, valid targets reduced the amplitude of the inhibitory P1 over the hemisphere contralateral to the no-target side whereas invalid targets enhanced the amplitude of the same inhibitory component. Enhanced inhibition was matched with speeded reorienting to invalid targets and drop in attentional costs. These findings show that reorienting of attention is modulated by the combination of cue-related facilitatory and target-related inhibitory activity.

Changes in predictive cuing modulate the hemispheric distribution of the P1 inhibitory response to attentional targets.

Brain activity related to orienting of attention with spatial cues and brain responses to attentional targets are influenced the probabilistic contingency between cues and targets. Compared to predictive cues, cues predicting at chance the location of targets reduce the filtering out of uncued locations and the costs in reorienting attention to targets presented at these locations. Slagter et al. (2016) have recently suggested that the larger target related P1 component that is found in the hemisphere ipsilateral to validly cued targets reflects stimulus-driven inhibition in the processing of the unstimulated side of space contralateral to the same hemisphere. Here we verified whether the strength of this inhibition and the amplitude of the corresponding P1 wave are modulated by the probabilistic link between cues and targets. Healthy participants performed a task of endogenous orienting once with predictive and once with non-predictive directional cues. In the non-predictive condition we observed a drop in the amplitude of the P1 ipsilateral to the target and in the costs of reorienting. No change in the inter-hemispheric latencies of the P1 was found between the two predictive conditions. The N1 facilitatory component was unaffected by predictive cuing. These results show that the predictive context modulates the strength of the inhibitory P1 response and that this modulation is not matched with changes in the inter-hemispheric interaction between the P1 generators of the two hemispheres.