Transcutaneous cervical vagus nerve stimulation improves sensory performance in humans: a randomized controlled crossover pilot study.

Accurate senses depend on high-fidelity encoding by sensory receptors and error-free processing in the brain. Progress has been made towards restoring damaged sensory receptors. However, methods for on-demand treatment of impaired central sensory processing are scarce. Prior invasive studies demonstrated that continuous vagus nerve stimulation (VNS) in rodents can activate the locus coeruleus-norepinephrine system to rapidly improve central sensory processing. Here, we investigated whether transcutaneous VNS improves sensory performance in humans. We conducted three sham-controlled experiments, each with 12 neurotypical adults, that measured the effects of transcutaneous VNS on metrics of auditory and visual performance, and heart rate variability (HRV). Continuous stimulation was delivered to cervical (tcVNS) or auricular (taVNS) branches of the vagus nerve while participants performed psychophysics tasks or passively viewed a display. Relative to sham stimulation, tcVNS improved auditory performance by 37% (p = 0.00052) and visual performance by 23% (p = 0.038). Participants with lower performance during sham conditions experienced larger tcVNS-evoked improvements (p = 0.0040). Lastly, tcVNS increased HRV during passive viewing, corroborating vagal engagement. No evidence for an effect of taVNS was observed. These findings validate the effectiveness of tcVNS in humans and position it as a method for on-demand interventions of impairments associated with central sensory processing dysfunction.

Transcutaneous cervical vagus nerve stimulation improves sensory performance in humans.

Accurate senses depend on high-fidelity encoding by sensory receptors and error-free processing in the brain. Progress has been made towards restoring damaged sensory receptors. However, methods for on-demand treatment of impaired central sensory processing are scarce. Prior invasive studies demonstrated that continuous vagus nerve stimulation (VNS) in rodents can activate the locus coeruleus-norepinephrine system to rapidly improve central sensory processing. Here, we investigated whether transcutaneous VNS improves sensory performance in humans. We conducted three sham-controlled experiments, each with 12 neurotypical adults, that measured the effects of transcutaneous VNS on metrics of auditory and visual performance, and heart rate variability (HRV). Continuous stimulation was delivered to cervical (tcVNS) or auricular (taVNS) branches of the vagus nerve while participants performed psychophysics tasks or passively viewed a display. Relative to sham stimulation, tcVNS improved auditory performance by 37% (p=0.00052) and visual performance by 23% (p=0.038). Participants with lower performance during sham conditions experienced larger tcVNS-evoked improvements (p=0.0040). Lastly, tcVNS increased HRV during passive viewing, corroborating vagal engagement. No evidence for an effect of taVNS was observed. These findings validate the effectiveness of tcVNS in humans and position it as a method for on-demand interventions of impairments associated with central sensory processing dysfunction.

Cortical magnification eliminates differences in contrast sensitivity across but not around the visual field.

Human visual performance changes dramatically both across (eccentricity) and around (polar angle) the visual field. Performance is better at the fovea, decreases with eccentricity, and is better along the horizontal than vertical meridian and along the lower than the upper vertical meridian. However, all neurophysiological and virtually all behavioral studies of cortical magnification have investigated eccentricity effects without considering polar angle. Most performance differences due to eccentricity are eliminated when stimulus size is cortically magnified (M-scaled) to equate the size of its cortical representation in primary visual cortex (V1). But does cortical magnification underlie performance differences around the visual field? Here, to assess contrast sensitivity, human adult observers performed an orientation discrimination task with constant stimulus size at different locations as well as when stimulus size was M-scaled according to stimulus eccentricity and polar angle location. We found that although M-scaling stimulus size eliminates differences across eccentricity, it does not eliminate differences around the polar angle. This finding indicates that limits in contrast sensitivity across eccentricity and around polar angle of the visual field are mediated by different anatomical and computational constraints.

An image-computable model of how endogenous and exogenous attention differentially alter visual perception.

Attention alters perception across the visual field. Typically, endogenous (voluntary) and exogenous (involuntary) attention similarly improve performance in many visual tasks, but they have differential effects in some tasks. Extant models of visual attention assume that the effects of these two types of attention are identical and consequently do not explain differences between them. Here, we develop a model of spatial resolution and attention that distinguishes between endogenous and exogenous attention. We focus on texture-based segmentation as a model system because it has revealed a clear dissociation between both attention types. For a texture for which performance peaks at parafoveal locations, endogenous attention improves performance across eccentricity, whereas exogenous attention improves performance where the resolution is low (peripheral locations) but impairs it where the resolution is high (foveal locations) for the scale of the texture. Our model emulates sensory encoding to segment figures from their background and predict behavioral performance. To explain attentional effects, endogenous and exogenous attention require separate operating regimes across visual detail (spatial frequency). Our model reproduces behavioral performance across several experiments and simultaneously resolves three unexplained phenomena: 1) the parafoveal advantage in segmentation, 2) the uniform improvements across eccentricity by endogenous attention, and 3) the peripheral improvements and foveal impairments by exogenous attention. Overall, we unveil a computational dissociation between each attention type and provide a generalizable framework for predicting their effects on perception across the visual field.

Differential impact of exogenous and endogenous attention on the contrast sensitivity function across eccentricity.

Both exogenous and endogenous covert spatial attention enhance contrast sensitivity, a fundamental measure of visual function that depends substantially on the spatial frequency and eccentricity of a stimulus. Whether and how each type of attention systematically improves contrast sensitivity across spatial frequency and eccentricity are fundamental to our understanding of visual perception. Previous studies have assessed the effects of spatial attention at individual spatial frequencies and, separately, at different eccentricities, but this is the first study to do so parametrically with the same task and observers. Using an orientation discrimination task, we investigated the effect of attention on contrast sensitivity over a wide range of spatial frequencies and eccentricities. Targets were presented alone or among distractors to assess signal enhancement and distractor suppression mechanisms of spatial attention. At each eccentricity, we found that exogenous attention preferentially enhanced spatial frequencies higher than the peak frequency in the baseline condition. In contrast, endogenous attention similarly enhanced a broad range of lower and higher spatial frequencies. The presence or absence of distractors did not alter the pattern of enhancement by each type of attention. Our findings reveal how the two types of covert spatial attention differentially shape how we perceive basic visual dimensions across the visual field.

Attention alters spatial resolution by modulating second-order processing.

Endogenous and exogenous visuospatial attention both alter spatial resolution, but they operate via distinct mechanisms. In texture segmentation tasks, exogenous attention inflexibly increases resolution even when detrimental for the task at hand and does so by modulating second-order processing. Endogenous attention is more flexible and modulates resolution to benefit performance according to task demands, but it is unknown whether it also operates at the second-order level. To answer this question, we measured performance on a second-order texture segmentation task while independently manipulating endogenous and exogenous attention. Observers discriminated a second-order texture target at several eccentricities. We found that endogenous attention improved performance uniformly across eccentricity, suggesting a flexible mechanism that can increase or decrease resolution based on task demands. In contrast, exogenous attention improved performance in the periphery but impaired it at central retinal locations, consistent with an inflexible resolution enhancement. Our results reveal that endogenous and exogenous attention both alter spatial resolution by differentially modulating second-order processing.

Neural Determinants of Task Performance during Feature-Based Attention in Human Cortex.

Studies of feature-based attention have associated activity in a dorsal frontoparietal network with putative attentional priority signals. Yet, how this neural activity mediates attentional selection and whether it guides behavior are fundamental questions that require investigation. We reasoned that endogenous fluctuations in the quality of attentional priority should influence task performance. Human subjects detected a speed increment while viewing clockwise (CW) or counterclockwise (CCW) motion (baseline task) or while attending to either direction amid distracters (attention task). In an fMRI experiment, direction-specific neural pattern similarity between the baseline task and the attention task revealed a higher level of similarity for correct than incorrect trials in frontoparietal regions. Using transcranial magnetic stimulation (TMS), we disrupted posterior parietal cortex (PPC) and found a selective deficit in the attention task, but not in the baseline task, demonstrating the necessity of this cortical area during feature-based attention. These results reveal that frontoparietal areas maintain attentional priority that facilitates successful behavioral selection.

Limits in feature-based attention to multiple colors.

Attention to a feature enhances the sensory representation of that feature. Although much has been learned about the properties of attentional modulation when attending to a single feature, the effectiveness of attending to multiple features is not well understood. We investigated this question in a series of experiments using a color-detection task while varying the number of attended colors in a cueing paradigm. Observers were shown either a single cue, two cues, or no cue (baseline) before detecting a coherent color target. We measured detection threshold by varying the coherence level of the target. Compared to the baseline condition, we found consistent facilitation of detection performance in the one-cue and two-cue conditions, but performance in the two-cue condition was lower than that in the one-cue condition. In the final experiment, we presented a 50% valid cue to emulate the situation in which observers were only able to attend a single color in the two-cue condition, and found equivalent detection thresholds with the standard two-cue condition. These results indicate a limit in attending to two colors and further imply that observers could effectively attend a single color at a time. Such a limit is likely due to an inability to maintain multiple active attentional templates for colors.

Limited featured-based attention to multiple features.

Attending to a feature (e.g., color or motion direction) can enhance the early visual processing of that feature. However, it is not known whether one can simultaneously enhance multiple features. We examined people's ability to attend to multiple features in a feature cueing paradigm. Each trial contained two intervals consisting of a random dot motion stimulus. One interval (noise) had 0% coherence (no net motion), while the other interval (signal) moved in a particular direction with varying levels of coherence. Participants reported which interval contained the signal in one of three cueing conditions. In the one-cue condition, a line segment preceded the stimuli indicating the direction of the signal with 100% validity. In the two-cue condition, two lines preceded the stimuli, indicating the signal would move in one of the two cued directions. In the no-cue condition, no line segment appeared before the dot stimuli. In several experiments, we consistently observed a lower detection threshold in the one-cue condition than the no-cue condition, showing that participants can enhance processing of a single feature. However, detection threshold was consistently higher for the two-cue than one-cue condition, indicating that participants could not simultaneously enhance two motion directions as effectively as one direction. This finding revealed a severe capacity limit in our ability to enhance early visual processing for multiple features.