Activation of primate frontal eye fields with a CMUT phased array system.

BACKGROUND: There are pushes toward non-invasive stimulation of neural tissues to prevent issues that arise from invasive brain recordings and stimulation. Transcranial Focused Ultrasound (TFUS) has been examined as a way to stimulate non-invasively, but previous studies have limitations in the application of TFUS. As a result, refinement is needed to improve stimulation results. NEW METHOD: We utilized a custom-built capacitive micromachined ultrasonic transducer (CMUT) that would send ultrasonic waves through skin and skull to targets located in the Frontal Eye Fields (FEF) region triangulated from co-registered MRI and CT scans while a non-human primate subject was performing a discrimination behavioral task. RESULTS: We observed that the stimulation immediately caused changes in the local field potential (LFP) signal that continued until stimulation ended, at which point there was higher voltage upon the cue for the animal to saccade. This co-incided with increases in activity in the alpha band during stimulation. The activity rebounded mid-way through our electrode-shank, indicating a specific point of stimulation along the shank. We observed different LFP signals for different stimulation targets, indicating the ability to"steer" the stimulation through the transducer. We also observed a bias in first saccades towards the opposite direction. CONCLUSIONS: In conclusion, we provide a new approach for non-invasive stimulation during performance of a behavioral task. With the ability to steer stimulation patterns and target using a large amount of transducers, the ability to provide non-invasive stimulation will be greatly improved for future clinical and research applications.

Frontal eye fields in macaque monkeys: prefrontal and premotor contributions to visually guided saccades.

Neuronal spiking was sampled from the frontal eye field (FEF) and from the rostral part of area 6 that reaches to the superior limb of the arcuate sulcus, dorsal to the arcuate spur when present (F2vr) in macaque monkeys performing memory-guided saccades and visually guided saccades for visual search. Neuronal spiking modulation in F2vr resembled that in FEF in many but not all respects. A new consensus clustering algorithm of neuronal modulation patterns revealed that F2vr and FEF contain a greater variety of modulation patterns than previously reported. The areas differ in the proportions of visuomotor neuron types, the proportions of neurons discriminating a target from distractors during visual search, and the consistency of modulation patterns across tasks. However, between F2vr and FEF we found no difference in the magnitude of delay period activity, the timing of the peak discharge rate relative to saccades, or the time of search target selection. The observed similarities and differences between the 2 cortical regions contribute to other work establishing the organization of eye fields in the frontal lobe and may help explain why FEF in monkeys is identified within granular prefrontal area 8 but in humans is identified within agranular premotor area 6.

Binocular Suppression in the Macaque Lateral Geniculate Nucleus Reveals Early Competitive Interactions between the Eyes.

The lateral geniculate nucleus (LGN) of the dorsal thalamus is the primary recipient of the two eyes' outputs. Most LGN neurons are monocular in that they are activated by visual stimulation through only one (dominant) eye. However, there are both intrinsic connections and inputs from binocular structures to the LGN that could provide these neurons with signals originating from the other (non-dominant) eye. Indeed, previous work introducing luminance differences across the eyes or using a single-contrast stimulus showed binocular modulation for single unit activity in anesthetized macaques and multiunit activity in awake macaques. Here, we sought to determine the influence of contrast viewed by both the non-dominant and dominant eyes on LGN single-unit responses in awake macaques. To do this, we adjusted each eye's signal strength by independently varying the contrast of stimuli presented to the two eyes. Specifically, we recorded LGN single unit spiking activity in two awake macaques while they viewed drifting gratings of varying contrast. We found that LGN neurons of all types [parvocellular (P), magnocellular (M), and koniocellular (K)] were significantly suppressed when stimuli were presented at low contrast to the dominant eye and at high contrast to the non-dominant eye. Further, the inputs of the two eyes showed antagonistic interaction, whereby the magnitude of binocular suppression diminished with high contrast in the dominant eye, or low contrast in the non-dominant eye. These results suggest that the LGN represents a site of precortical binocular processing involved in resolving discrepant contrast differences between the eyes.

Visuomotor Transformations Are Modulated by Focused Ultrasound over Frontal Eye Field.

Neuromodulation with focused ultrasound (FUS) is being widely explored as a non-invasive tool to stimulate focal brain regions because of its superior spatial resolution and coverage compared with other neuromodulation methods. The precise effects of FUS stimulation on specific regions of the brain are not yet fully understood. Here, we characterized the behavioral effects of FUS stimulation directly applied through a craniotomy over the macaque frontal eye field (FEF). In macaque monkeys making directed eye movements to perform visual search tasks with direct or arbitrary responses, focused ultrasound was applied through a craniotomy over the FEF. Saccade response times (RTs) and error rates were determined for trials without or with FUS stimulation with pulses at a peak negative pressure of either 250 or 425 kPa. Both RTs and error rates were affected by FUS. Responses toward a target located contralateral to the FUS stimulation were approximately 3 ms slower in the presence of FUS in both monkeys studied, while only one exhibited a slowing of responses for ipsilateral targets. Error rates were lower in one monkey in this study. In another search task requiring making eye movements toward a target (pro-saccades) or in the opposite direction (anti-saccades), the RT for pro-saccades increased in the presence of FUS stimulation. Our results indicate the effectiveness of FUS to modulate saccadic responses when stimulating FEF in awake, behaving non-human primates.

Prefrontal Control of Visual Distraction.

Avoiding distraction by conspicuous but irrelevant stimuli is critical to accomplishing daily tasks. Regions of prefrontal cortex control attention by enhancing the representation of task-relevant information in sensory cortex, which can be measured in modulation of both single neurons and event-related electrical potentials (ERPs) on the cranial surface [1, 2]. When irrelevant information is particularly conspicuous, it can distract attention and interfere with the selection of behaviorally relevant information. Such distraction can be minimized via top-down control [3-5], but the cognitive and neural mechanisms giving rise to this control over distraction remain uncertain and debated [6-9]. Bridging neurophysiology to electrophysiology, we simultaneously recorded neurons in prefrontal cortex and ERPs over extrastriate visual cortex to track the processing of salient distractors during a visual search task. Critically, when the salient distractor was successfully ignored, but not otherwise, we observed robust suppression of salient distractor representations. Like target selection, the distractor suppression was observed in prefrontal cortex before it appeared over extrastriate cortical areas. Furthermore, all prefrontal neurons that showed suppression of the task-irrelevant distractor also contributed to selecting the target. This suggests a common prefrontal mechanism is responsible for both selecting task-relevant and suppressing task-irrelevant information in sensory cortex. Taken together, our results resolve a long-standing debate over the mechanisms that prevent distraction, and provide the first evidence directly linking suppressed neural firing in prefrontal cortex with surface ERP measures of distractor suppression.

Neural structures involved in visual search guidance by reward-enhanced contextual cueing of the target location.

Spatial contextual cueing reflects an incidental form of learning that occurs when spatial distractor configurations are repeated in visual search displays. Recently, it was reported that the efficiency of contextual cueing can be modulated by reward. We replicated this behavioral finding and investigated its neural basis with fMRI. Reward value was associated with repeated displays in a learning session. The effect of reward value on context-guided visual search was assessed in a subsequent fMRI session without reward. Structures known to support explicit reward valuation, such as ventral frontomedial cortex and posterior cingulate cortex, were modulated by incidental reward learning. Contextual cueing, leading to more efficient search, went along with decreased activation in the visual search network. Retrosplenial cortex played a special role in that it showed both a main effect of reward and a reward×configuration interaction and may thereby be a central structure for the reward modulation of context-guided visual search.

The right temporo-parietal junction contributes to visual feature binding.

We investigated the neural basis of conjoined processing of color and spatial frequency with functional magnetic resonance imaging (fMRI). A multivariate classification algorithm was trained to differentiate between either isolated color or spatial frequency differences, or between conjoint differences in both feature dimensions. All displays were presented in a singleton search task, avoiding confounds between conjunctive feature processing and search difficulty that arose in previous studies contrasting single feature and conjunction search tasks. Based on patient studies, we expected the right temporo-parietal junction (TPJ) to be involved in conjunctive feature processing. This hypothesis was confirmed in that only conjoined color and spatial frequency differences, but not isolated feature differences could be classified above chance level in this area. Furthermore, we could show that the accuracy of a classification of differences in both feature dimensions was superadditive compared to the classification accuracies of isolated color or spatial frequency differences within the right TPJ. These data provide evidence for the processing of feature conjunctions, here color and spatial frequency, in the right TPJ.

A high-resolution 7-Tesla fMRI dataset from complex natural stimulation with an audio movie.

Here we present a high-resolution functional magnetic resonance (fMRI) dataset - 20 participants recorded at high field strength (7 Tesla) during prolonged stimulation with an auditory feature film ("Forrest Gump"). In addition, a comprehensive set of auxiliary data (T1w, T2w, DTI, susceptibility-weighted image, angiography) as well as measurements to assess technical and physiological noise components have been acquired. An initial analysis confirms that these data can be used to study common and idiosyncratic brain response patterns to complex auditory stimulation. Among the potential uses of this dataset are the study of auditory attention and cognition, language and music perception, and social perception. The auxiliary measurements enable a large variety of additional analysis strategies that relate functional response patterns to structural properties of the brain. Alongside the acquired data, we provide source code and detailed information on all employed procedures - from stimulus creation to data analysis. In order to facilitate replicative and derived works, only free and open-source software was utilized.

Evidence for feature binding in the superior parietal lobule.

The neural substrates of feature binding are an old, yet still not completely resolved problem. While patient studies suggest that posterior parietal cortex is necessary for feature binding, imaging evidence has been inconclusive in the past. These studies compared visual feature and conjunction search to investigate the neural substrate of feature conjunctions. However, a common problem of these comparisons was a confound with search difficulty. To circumvent this confound, we directly investigated the localized representation of features (color and spatial frequency) and feature conjunctions in a single search task by using multivariate pattern analysis at high field strength (7T). In right superior parietal lobule, we found evidence for the representation of feature conjunctions that could not be explained by the summation of individual feature representations and thus indicates conjoined processing of color and spatial frequency.

Speed change detection in foveal and peripheral vision.

Perception of constant motion has been extensively studied both psychophysically and physiologically, but the human ability to detect dynamic changes in motion, such as rapid speed changes, is only poorly characterized and understood. Yet, perception and representation of such dynamic changes is of strong behavioral relevance, as illustrated by their potential for attentional capture. In the present study, we measured and compared detection thresholds for instantaneous accelerations and decelerations of drifting Gabor patches at different retinal eccentricities. As a main result, we find that detection performance depends strongly on eccentricity. Under foveal viewing conditions, average thresholds were lower for accelerations than for decelerations. However, between 5° and 15° eccentricity, this relation is inverted, and deceleration detection becomes better than acceleration detection. Results of an additional experiment suggest that this can be explained by a fast eccentricity-dependent adaptation effect. Our findings are discussed with special emphasis on their relation to data from neurophysiological experiments.