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Ben Hamed, S.

Publications and source records attributed to Ben Hamed, S..

25 records · Page 2Linked to original sources

Selection and suppression of visual information in the macaque prefrontal cortex

In everyday life, we are continuously struggling at focusing on our current goals while at the same time avoiding distractions. Attention is the neuro-cognitive process devoted to the selection of behaviorally relevant sensory information while at the same time preventing distraction by irrelevant information. Visual selection can be implemented by both long-term (learning-based spatial prioritization) and short term (dynamic spatial attention) mechanisms. On the other hand, distraction can be prevented proactively, by strategically prioritizing task-relevant information at the expense of irrelevant information, or reactively, by actively suppressing the processing of distractors. The distinctive neuronal signature of each of these four processes is largely unknown. Likewise, how selection and suppression mechanisms interact to drive perception has never been explored neither at the behavioral nor at the neuronal level. Here, we apply machine-learning decoding methods to prefrontal cortical (PFC) activity to monitor dynamic spatial attention with an unprecedented spatial and temporal resolution. This leads to several novel observations. We first identify independent behavioral and neuronal signatures for learning-based attention prioritization and dynamic attentional selection. Second, we identify distinct behavioral and neuronal signatures for proactive and reactive suppression mechanisms. We find that while distracting task-relevant information is suppressed proactively, task-irrelevant information is suppressed reactively. Critically, we show that distractor suppression, whether proactive or reactive, strongly depends on both learning-based attention prioritization and dynamic attentional selection. Overall, we thus provide a unified neuro-cognitive framework describing how the prefrontal cortex implements spatial selection and distractor suppression in order to flexibly optimize behavior in dynamic environments.

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Rhythmic variations in prefrontal inter-neuronal correlations, their underlying mechanisms and their behavioral correlates

Functional neuronal correlations between pairs of neurons are thought to play an important role in neuronal information processing and optimal neuronal computations during attention, perception, decision-making and learning. These noise correlations are often assumed to be stable in time. However, recent studies suggest that cognitive processes are rhythmic, this rhythmicity accounting for variations in overt behavioral performance. Whether this rhythmicity coincides with variations in shared noise variability is unknown. Here, we perform simultaneous recordings from the macaque frontal eye fields, while animals are engaged in a spatial memory task. We report that noise correlations in prefrontal cortex fluctuate rhythmically in the high alpha (10-16Hz) and beta (20-30Hz) frequency ranges. Importantly, these rhythmic modulations in shared neuronal variability account for dynamic changes in overt behavioral performance. They also coincide with increased spike-LFP phase coupling in these specific frequency ranges, the spatial profile of which vary between superficial and deep cortical layers. Finally, we demonstrate, using an artificial neuronal model, that rhythmic variations in noise correlation oscillations parsimoniously arise from long range (LFP) and local spike-LFP phase coupling mechanisms. Thus a significant portion of noise correlation fluctuations can be attributed to long-range global network rhythmicity.

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Prefrontal attentional saccades explore space at an alpha rhythm

Recent studies suggest that attention samples space rhythmically through oscillatory interactions in the frontoparietal network. However, the precise mechanism through which the prefrontal cortex, at the source of attention control signals, organizes this rhythmic exploration of space remains unknown. We show that, when decoded at a high spatial (0.1{degrees}) and temporal resolution (50ms), the prefrontal covert attentional spotlight, aka the minds eye, continuously explores space at an alpha 7-12 Hz rhythm. When sensory events are presented at a specific optimal phase (resp. anti-phase) with respect to this rhythm, sensory encoding and behavioral report are accurate (resp. poor). We propose that this rhythmic prefrontal attentional spotlight dynamics corresponds to a continuous overt exploration of space via alpha-clocked attentional saccades. These attentional saccades are highly flexible, their pattern of space exploration depending both on within-trial and across-task contingencies. These results are discussed in the context of exploration and exploitation strategies and prefrontal top-down attentional control.\n\nHighlightsO_LIThe decoded prefrontal attentional spotlight samples visual space in rhythmic cycles\nC_LIO_LIThis rhythmic attentional exploration predicts neuronal sensory processing accuracy\nC_LIO_LIThis rhythmic attentional exploration predicts overt behavioral accuracy\nC_LIO_LIThese rhythmic cycles define alpha-clocked attentional saccades\nC_LIO_LISpace exploration by attentional saccades is highly flexible and under top-down control\nC_LI

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Interneuronal correlations dynamically adjust to task demands at multiple time-scales

Functional neuronal correlations between pairs of neurons are thought to play an important role in neuronal information processing and optimal neuronal computations during attention, perception, decision-making and learning. Here, we report dynamic changes in prefrontal neuronal noise correlations at multiple time-scales, as a function of task contingencies. Specifically, we record neuronal activity from the macaque frontal eye fields, a cortical region at the source of spatial attention top-down control, while the animals are engaged in tasks of varying cognitive demands. First, we show that noise correlations decrease as cognitive engagement and task demands increase, both across tasks and within-trials. Second, we demonstrate, for the first time, rhythmic modulations of noise correlations in the alpha and beta frequency ranges that account both for overt behavioral performance and for layer specific modulations in spike-field coherence. All this taken together demonstrates a strong functional role of noise correlations in cognitive flexibility.

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Norepinephrine improves attentional orienting in a predictive context

The role of norepinephrine (NE) in visuo-spatial attention remains poorly understood. Our goal was to identify the attentional processes under the influence of NE and to characterize these influences. We tested the effects of atomoxetine injections (ATX), a NE-reuptake inhibitor that boosts the level of NE in the brain, on seven monkeys performing a saccadic cued task in which cues and distractors were used to manipulate spatial attention. We found that when the cue accurately predicted the location of the upcoming cue in 80% of the trials, ATX consistently improved attentional orienting, as measured from reaction times (RTs). These effects were best accounted for by a faster accumulation rate in the valid trials, rather than by a change in the decision threshold. By contrast, the effect of ATX on alerting and distractor interference was more mitigated. Finally, we also found that, under ATX, RTs to non-cued targets were longer when these were presented separately from cued targets. This suggests that the impact of NE on visuo-spatial attention depends on the context, such that the adaptive changes elicited by the highly informative value of the cues in the most frequent trials were accompanied by a cost in the less frequent trials.

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Neuronal population correlates of target selection and distractor filtering

Frontal Eye Field (FEF) single-cell neuronal activity discriminates between relevant and irrelevant visual stimuli and its magnitude has been shown to predict conscious perception. How this is reflected at the population level in terms of spatial codes is unknown. We recorded neuronal population activity in the FEF while monkeys were performing a forced choice cued detection task with identical target and distractor stimuli. Using machine learning techniques, we quantified information about the spatial estimate of targets and distracters in the FEF population activity and we analyzed how these relate to the report of perception. We found that the FEF population activity provides a precise estimate of the spatial location of perception. This estimate doesnt necessarily match the actual physical world. Importantly, the closer this prefrontal population estimate is to the veridical spatial information, the higher the probability that the stimulus was reported as perceived. This was observed both when the reported stimulus was a target (i.e. correct detection trials) or a distractor (i.e. false alarm trials). Overall, we thus show that how and what we perceive of our environments depends on the precision with which this environment is coded by prefrontal neuronal populations.

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Cortical networks for encoding near and far space in the non-human primate

While extra-personal space is often erroneously considered as a unique entity, early neuropsychological studies report a dissociation between near and far space processing both in humans and in monkeys. Here, we use functional MRI in a naturalistic 3D environment to describe the non-human primate near and far space cortical networks. We describe the co-occurrence of two extended functional networks respectively dedicated to near and far space processing. Specifically, far space processing involves occipital, temporal, parietal, posterior cingulate as well as orbitofrontal regions not activated by near space, possibly subserving the processing of the shape and identity of objects. In contrast, near space processing involves temporal, parietal and prefrontal regions not activated by far space, possibly subserving the preparation of an arm/hand mediated action in this proximal space. Interestingly, this network also involves somatosensory regions, suggesting a cross-modal anticipation of touch by a nearby object. Last, we also describe cortical regions that process both far and near space with a preference for one or the other. This suggests a continuous encoding of relative distance to the body, in the form of a far-to-near gradient. We propose that these cortical gradients in space representation subserve the physically delineable peripersonal spaces described in numerous psychology and psychophysics studies.\n\nHighlightsO_LINear space processing involves temporal, parietal and prefrontal regions.\nC_LIO_LIFar space activates occipital, temporal, parietal, cingulate & orbitofrontal areas.\nC_LIO_LIMost regions process both far & near space, with a preference for one or the other.\nC_LIO_LIFar-to-near gradient may subserve behavioral changes in peripersonal space size.\nC_LI

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