Sensory Competition Research Articles

Neural Basis of Biased Competition in Development: Sensory Competition in Visual Cortex of School-Aged Children.

The fundamental receptive field (RF) architecture in human visual cortex becomes adult-like by age 5. However, visuo-spatial functions continue to develop until teenage years. This suggests that, despite the early maturation of the RF structure, functional interactions within and across RFs may mature slowly. Here, we used fMRI to investigate functional interactions among multiple stimuli in the visual cortex of school children (ages 8 to 12) in the context of biased competition theory. In the adult visual system, multiple objects presented in the same visual field compete for neural representation. These competitive interactions occur at the level of the RF and are therefore closely linked to the RF architecture. Like in adults, we found suppression of evoked responses in children's visual cortex when multiple stimuli were presented simultaneously. Such suppression effects were modulated by the spatial distance between the stimuli as a function of RF size across the visual system. Our findings suggest that basic competitive interactions in the visual cortex of children above age 8 operate in an adult-like manner, with subtle differences in early visual areas and area MT. Our study establishes a paradigm and provides baseline data to investigate the neural basis of visuo-spatial processing in typical and atypical development.

Fear Spreading Across Senses: Visual Emotional Events Alter Cortical Responses to Touch, Audition, and Vision.

Attention and perception are potentiated for emotionally significant stimuli, promoting efficient reactivity and survival. But does such enhancement extend to stimuli simultaneously presented across different sensory modalities? We used functional magnetic resonance imaging in humans to examine the effects of visual emotional signals on concomitant sensory inputs in auditory, somatosensory, and visual modalities. First, we identified sensory areas responsive to task-irrelevant tones, touches, or flickers, presented bilaterally while participants attended to either a neutral or a fearful face. Then, we measured whether these responses were modulated by the emotional content of the face. Sensory responses in primary cortices were enhanced for auditory and tactile stimuli when these appeared with fearful faces, compared with neutral, but striate cortex responses to the visual stimuli were reduced in the left hemisphere, plausibly as a consequence of sensory competition. Finally, conjunction and functional connectivity analyses identified 2 distinct networks presumably responsible for these emotional modulatory processes, involving cingulate, insular, and orbitofrontal cortices for the increased sensory responses, and ventrolateral prefrontal cortex for the decreased sensory responses. These results suggest that emotion tunes the excitability of sensory systems across multiple modalities simultaneously, allowing the individual to adaptively process incoming inputs in a potentially threatening environment.

Selective disinhibition: A unified neural mechanism for predictive and post hoc attentional selection

The natural world presents us with a rich and ever-changing sensory landscape containing diverse stimuli that constantly compete for representation in the brain. When the brain selects a stimulus as the highest priority for attention, it differentially enhances the representation of the selected, “target” stimulus and suppresses the processing of other, distracting stimuli. A stimulus may be selected for attention while it is still present in the visual scene (predictive selection) or after it has vanished (post hoc selection). We present a biologically inspired computational model that accounts for the prioritized processing of information about targets that are selected for attention either predictively or post hoc. Central to the model is the neurobiological mechanism of “selective disinhibition” – the selective suppression of inhibition of the representation of the target stimulus. We demonstrate that this mechanism explains major neurophysiological hallmarks of selective attention, including multiplicative neural gain, increased inter-trial reliability (decreased variability), and reduced noise correlations. The same mechanism also reproduces key behavioral hallmarks associated with target-distracter interactions. Selective disinhibition exhibits several distinguishing and advantageous features over alternative mechanisms for implementing target selection, and is capable of explaining the effects of selective attention over a broad range of real-world conditions, involving both predictive and post hoc biasing of sensory competition and decisions.

Sustained selective attention to competing amplitude-modulations in human auditory cortex.

Auditory selective attention plays an essential role for identifying sounds of interest in a scene, but the neural underpinnings are still incompletely understood. Recent findings demonstrate that neural activity that is time-locked to a particular amplitude-modulation (AM) is enhanced in the auditory cortex when the modulated stream of sounds is selectively attended to under sensory competition with other streams. However, the target sounds used in the previous studies differed not only in their AM, but also in other sound features, such as carrier frequency or location. Thus, it remains uncertain whether the observed enhancements reflect AM-selective attention. The present study aims at dissociating the effect of AM frequency on response enhancement in auditory cortex by using an ongoing auditory stimulus that contains two competing targets differing exclusively in their AM frequency. Electroencephalography results showed a sustained response enhancement for auditory attention compared to visual attention, but not for AM-selective attention (attended AM frequency vs. ignored AM frequency). In contrast, the response to the ignored AM frequency was enhanced, although a brief trend toward response enhancement occurred during the initial 15 s. Together with the previous findings, these observations indicate that selective enhancement of attended AMs in auditory cortex is adaptive under sustained AM-selective attention. This finding has implications for our understanding of cortical mechanisms for feature-based attentional gain control.

Visual, auditory and tactile stimuli compete for early sensory processing capacities within but not between senses

We investigated whether unattended visual, auditory and tactile stimuli compete for capacity-limited early sensory processing across senses. In three experiments, we probed competitive audio-visual, visuo-tactile and audio-tactile stimulus interactions. To this end, continuous visual, auditory and tactile stimulus streams (‘reference’ stimuli) were frequency-tagged to elicit steady-state responses (SSRs). These electrophysiological oscillatory brain responses indexed ongoing stimulus processing in corresponding senses. To induce competition, we introduced transient frequency-tagged stimuli in same and/or different senses (‘competitors’) during reference presentation. Participants performed a separate visual discrimination task at central fixation to control for attentional biases of sensory processing. A comparison of reference-driven SSR amplitudes between competitor-present and competitor-absent periods revealed reduced amplitudes when a competitor was presented in the same sensory modality as the reference. Reduced amplitudes indicated the competitor's suppressive influence on reference stimulus processing. Crucially, no such suppression was found when a competitor was presented in a different than the reference modality. These results strongly suggest that early sensory competition is exclusively modality-specific and does not extend across senses. We discuss consequences of these findings for modeling the neural mechanisms underlying intermodal attention.

Electrophysiological correlates of visual adaptation and sensory competition

The face-sensitive evoked N170 component of the event related potential (ERP) is reduced if another face is presented before when compared to the previous presentation of a low-level control stimulus (phase-scrambled face). This effect is thought to reflect category-specific adaptation processes. Similarly, presenting two faces concurrently also reduces the N170, suggesting that stimuli compete for neural representations in the occipito-temporal cortex as early as 170ms. Here we compared the ERPs obtained for two faces or for a face and a phase-scrambled face in three different conditions: (1) a first stimulus (S1) followed by a second one (S2), similarly to previous adaptation paradigms; (2) S1 remaining on screen when S2 appeared, as previously used in studies of competition; (3) or S1 and S2 having simultaneous onset and offset as well. We found a significant and stimulus specific reduction of the N170 in both conditions where the onset of S1 preceded the onset of S2. In contrast, simultaneous presentation of the two stimuli had no specific effect on the ERPs at least until 200ms post-stimulus onset. This suggests either that competition does not lead to early repetition suppression or that the absence of a larger N170 response to two simultaneously presented face stimuli compared to a single stimulus reflects competition between overlapping representations. Overall, our results show that the asynchronous presentation of S1 and S2 is critical to observe stimulus specific reduction of the N170, presumably reflecting adaptation-related processes.

The parietal cortex and saccade planning: lessons from human lesion studies.

The parietal cortex is a critical interface for attention and integration of multiple sensory signals that can be used for the implementation of motor plans. Many neurons in this region exhibit strong attention-, reach-, grasp- or saccade-related activity. Here, we review human lesion studies supporting the critical role of the parietal cortex in saccade planning. Studies of patients with unilateral parietal damage and spatial neglect reveal characteristic spatially lateralized deficits of saccade programming when multiple stimuli compete for attention. However, these patients also show bilateral impairments of saccade initiation and control that are difficult to explain in the context of their lateralized deficits of visual attention. These findings are reminiscent of the deficits of oculomotor control observed in patients with Bálint's syndrome consecutive to bilateral parietal damage. We propose that some oculomotor deficits following parietal damage are compatible with a decisive role of the parietal cortex in saccade planning under conditions of sensory competition, while other deficits reflect disinhibition of low-level structures of the oculomotor network in the absence of top-down parietal modulation.

Functional lateralization in auditory cortex under informational masking and in silence

The N(1) m is an evoked magnetic field in auditory cortex that is automatically elicited by tones in silence but not in the context of multiple other tones: when listeners are unaware of a tone stream because of informational masking, no N(1) m-like activity is observed. In contrast, N(1) m-like activity is evoked when listeners are aware of the regular tone stream in the same context but in another trial. Here we compared this awareness-related negativity (ARN) with the automatic N(1) m. First, we evaluated whether stimulus lateralization by ear or interaural time differences modulates hemispheric lateralization of the response, as a putative marker of sensory processing. Second, we evaluated the stimulus-independent hemispheric balance thought to indicate higher level cortical processing. The results dissociate three, partly overlapping, time intervals: the P(1) m (45-85 ms) was evoked by missed and detected target tones alike. Subsequent negative activity was only observed when listeners indicated awareness of the target stream inside the multi-tone masker. In the N(1) m time interval (75-175 ms), hemispheric balance of the ARN and N(1) m was modulated by stimulus lateralization. In the subsequent time interval (175-275 ms), auditory-cortex activity was generally right-lateralized in silence and balanced under informational masking, but was not modulated by stimulus lateralization. These results suggest that the same auditory-cortex activity that varies with perceptual awareness also shows sensory response features. This is in accordance with models for visual perception, suggesting that sensory competition determines whether midlevel visual responses occur automatically or vary with perceptual state.

Sensory Competition in the Face Processing Areas of the Human Brain

The concurrent presentation of multiple stimuli in the visual field may trigger mutually suppressive interactions throughout the ventral visual stream. While several studies have been performed on sensory competition effects among non-face stimuli relatively little is known about the interactions in the human brain for multiple face stimuli. In the present study we analyzed the neuronal basis of sensory competition in an event-related functional magnetic resonance imaging (fMRI) study using multiple face stimuli. We varied the ratio of faces and phase-noise images within a composite display with a constant number of peripheral stimuli, thereby manipulating the competitive interactions between faces. For contralaterally presented stimuli we observed strong competition effects in the fusiform face area (FFA) bilaterally and in the right lateral occipital area (LOC), but not in the occipital face area (OFA), suggesting their different roles in sensory competition. When we increased the spatial distance among pairs of faces the magnitude of suppressive interactions was reduced in the FFA. Surprisingly, the magnitude of competition depended on the visual hemifield of the stimuli: ipsilateral stimulation reduced the competition effects somewhat in the right LOC while it increased them in the left LOC. This suggests a left hemifield dominance of sensory competition. Our results support the sensory competition theory in the processing of multiple faces and suggests that sensory competition occurs in several cortical areas in both cerebral hemispheres.

Studying Multisensory Processing and Its Role in the Representation of Space through Pathological and Physiological Crossmodal Extinction

The study of crossmodal extinction has brought a considerable contribution to our understanding of how the integration of stimuli perceived in multiple sensory modalities is used by the nervous system to build coherent representations of the space that directly surrounds us. Indeed, by revealing interferences between stimuli in a disturbed system, extinction provides an invaluable opportunity to investigate the interactions that normally exist between those stimuli in an intact system. Here, we first review studies on pathological crossmodal extinction, from the original demonstration of its existence, to its role in the exploration of the multisensory neural representation of space and the current theoretical accounts proposed to explain the mechanisms involved in extinction and multisensory competition. Then, in the second part of this paper, we report recent findings showing that physiological multisensory competition phenomena resembling clinical crossmodal extinction exist in the healthy brain. We propose that the development of a physiological model of sensory competition is fundamental to deepen our understanding of the cerebral mechanisms of multisensory perception and integration. In addition, a similar approach to develop a model of physiological sensory competition in non-human primates should allow combining functional neuroimaging with more invasive techniques, such as transient focal lesions, in order to bridge the gap between works done in the two species and at different levels of analysis.

Sensory competition in the face processing areas of the human brain

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Attentional learning: learning to bias sensory competition

Attentional learning: learning to bias sensory competition

Modality-Specific, Multitask Locomotor Deficits Persist Despite Good Recovery After a Traumatic Brain Injury

McFadyen BJ, Cantin J-F, Swaine B, Duchesneau G, Doyon J, Dumas D, Fait P. Modality-specific, multitask locomotor deficits persist despite good recovery after a traumatic brain injury. Objective To study the effects of sensory modality of simultaneous tasks during walking with and without obstacles after moderate to severe traumatic brain injury (TBI). Design Group comparison study. Setting Gait analysis laboratory within a postacute rehabilitation facility. Participants Volunteer sample (N=18). Persons with moderate to severe TBI (n=11) (9 men, 3 women; age, 37.56±13.79y) and a comparison group (n=7) of subjects without neurologic problems matched on average for body mass index and age (4 men, 3 women; age, 39.19±17.35y). Interventions Not applicable. Main Outcome Measures Magnitudes and variability for walking speeds, foot clearance margins (ratio of foot clearance distance to obstacle height), and response reaction times (both direct and as a relative cost because of obstacle avoidance). Results The TBI group had well-recovered walking speeds and a general ability to avoid obstacles. However, these subjects did show lower trail limb toe clearances ( P=.003) across all conditions. Response reaction times to the Stroop tasks were longer in general for the TBI group ( P=.017), and this group showed significant increases in response reaction times for the visual modality within the more challenging obstacle avoidance task that was not observed for control subjects. A measure of multitask costs related to differences in response reaction times between obstructed and unobstructed trials also only showed increased attention costs for the visual over the auditory stimuli for the TBI group ( P=.002). Conclusions Mobility is a complex construct, and the present results provide preliminary findings that, even after good locomotor recovery, subjects with moderate to severe TBI show residual locomotor deficits in multitasking. Furthermore, our results suggest that sensory modality is important, and greater multitask costs occur during sensory competition (ie, visual interference).

Electrophysiological Evidence for Temporal Dissociation between Spatial Attention and Sensory Competition during Human Face Processing

Scalp event-related potential (ERP) studies in humans indicate that face processes taking place between 130 and 170 ms after stimulus onset at posterior sites (N170) are strongly reduced when another face stimulus is processed concurrently or has been presented shortly before for a prolonged period. These observations suggest that neural representations of individual faces compete in the occipitotemporal cortex as early as 130 ms. Here, we tested the respective role of spatial attention and sensory competition in accounting for the amplitude reduction of the N170 during concurrent face stimulation. ERPs time locked to a lateralized face stimulus were recorded while subjects were fixating either a face or a controlled scrambled-face stimulus (context factor) and were engaged in either a high- or a low-attentional load task at fixation (task factor). The N170 amplitude to the lateralized face stimulus was reduced both when the central stimulus was a face compared with a scrambled face and when the attentional load at fixation was high. However, these effects of context and task factors were largely additive. Most importantly, spatial attention modulated visual processes as early as 80 ms after stimulus onset, whereas sensory competition effects started at about 130 ms. These results provide strong evidence that the N170 in response to faces is modulated by spatial attention, and also that spatial attention and sensory competition do not reflect the same mechanisms of early selection of visual information in the extrastriate cortex.

Peripheral Pathways Regulate Motoneuron Collateral Dynamics

Motor axons regenerating after repair of mixed nerve reinnervate pathways leading to muscle more often than those leading to skin [preferential motor reinnervation (PMR)]. Motoneurons that initially project collaterals to both muscle and skin prune incorrect projections to generate specificity. The number of motor axon collaterals maintained entirely within cutaneous or muscle pathways, however, is unknown. To overcome this shortcoming, dorsal root ganglion excision has been used to allow only motor axons to regenerate after a peripheral lesion. Motor axon number in reinnervated cutaneous and muscle pathways can then be correlated with the number of parent motoneurons determined by retrograde labeling. The number of collaterals per neuron can be calculated for each environment and the relative roles of pathway and end organ assessed by blocking the distal pathways to prevent target reinnervation. Without sensory competition, PMR develops in two stages: a limited response to muscle nerve and then a robust response to muscle that may involve retrograde signaling to the proximal pathway. Motoneurons maintain more collaterals in cutaneous nerve than in muscle nerve, even without muscle contact. This difference could result either from increased collateral formation in cutaneous nerve or from increased collateral pruning in muscle nerve. In either instance, these findings confirm that muscle and cutaneous pathways have functionally significant identities that can be recognized by motor axons and can regulate their arborization. Decreased arborization in muscle pathways could promote regeneration by focusing neuronal resources on high-yield projections; increased arborization in cutaneous pathways, conversely, would enhance pathfinding abilities.

Visuomotor links in awareness: evidence from extinction

In patients with extinction, ipsilesional stimuli may abolish awareness of contralesional stimuli. Explanations of extinction often assume a serial model of processing in which sensory competition and identification precedes the selection of responses. We tested the adequacy of this assumption by examining the effects of response variables on visual awareness in six patients using signal detection analysis. Ipsilesional stimuli modulated patients' response criteria in deciding whether a contralesional stimulus was a target, and response modality (verbal or motor) modulated patients' abilities to discriminate between contralesional targets and distractors. This pattern of input variables modulating response criteria and output variables modulating discriminability indicates the extent to which attentional and intentional systems are tightly intertwined, with bi-directional effects in producing visual awareness.

Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field.

Perceptual suppression of distractors may depend on both endogenous and exogenous factors, such as attentional load of the current task and sensory competition among simultaneous stimuli, respectively. We used functional magnetic resonance imaging (fMRI) to compare these two types of attentional effects and examine how they may interact in the human brain. We varied the attentional load of a visual monitoring task performed on a rapid stream at central fixation without altering the central stimuli themselves, while measuring the impact on fMRI responses to task-irrelevant peripheral checkerboards presented either unilaterally or bilaterally. Activations in visual cortex for irrelevant peripheral stimulation decreased with increasing attentional load at fixation. This relative decrease was present even in V1, but became larger for successive visual areas through to V4. Decreases in activation for contralateral peripheral checkerboards due to higher central load were more pronounced within retinotopic cortex corresponding to 'inner' peripheral locations relatively near the central targets than for more eccentric 'outer' locations, demonstrating a predominant suppression of nearby surround rather than strict 'tunnel vision' during higher task load at central fixation. Contralateral activations for peripheral stimulation in one hemifield were reduced by competition with concurrent stimulation in the other hemifield only in inferior parietal cortex, not in retinotopic areas of occipital visual cortex. In addition, central attentional load interacted with competition due to bilateral versus unilateral peripheral stimuli specifically in posterior parietal and fusiform regions. These results reveal that task-dependent attentional load, and interhemifield stimulus-competition, can produce distinct influences on the neural responses to peripheral visual stimuli within the human visual system. These distinct mechanisms in selective visual processing may be integrated within posterior parietal areas, rather than earlier occipital cortex.

The role of neural mechanisms of attention in solving the binding problem.

We thank L. Chelazzi, V. Ferrera, P. Fries, S. Kastner, and A. Rossi for helpful comments on the manuscript.