Optimal performance in a countermanding saccade task

To understand the neural mechanism of fixation, we investigated effects of electrical stimulation of the frontal eye field (FEF) and its vicinity on visually guided (Vsacs) and memory-guided saccades (Msacs) in trained monkeys and found that there were two types of suppression induced by the electrical stimulation: suppression of ipsilateral saccades and suppression of bilateral saccades. In this report, we characterized the properties of the suppression of bilateral Vsacs and Msacs. Stimulation of the bilateral suppression sites suppressed the initiation of both Vsacs and Msacs in all directions during and approximately 50 ms after stimulation but did not affect the vector of these saccades. The suppression was stronger for ipsiversive larger saccades and contraversive smaller saccades, and saccades with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for the suppression of ipsilateral and contralateral Vsacs was approximately 40-50 ms before saccade onset, indicating that the suppression occurred most likely in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of bilateral saccades were located in the prearcuate gyrus facing the inferior arcuate sulcus where stimulation induced suppression at < or =40 microA but usually did not evoke any saccades at 80 microA and were different from those of ipsilateral saccades where stimulation evoked saccades at < or =50 microA. The bilateral suppression sites contained fixation neurons. The results suggest that fixation neurons in the bilateral suppression area of the FEF may play roles in maintaining fixation by suppressing saccades in all directions.

1. Monkeys were trained to look to brief visual targets presented in a completely darkened room. On some trials, after the visual target disappeared but before a saccade to the target could be initiated, the eyes were driven to another position in the orbit by electrical stimulation of the superior colliculus. Retinocentric models of the saccadic system predict that a saccade with a predetermined distance and direction based entirely on retinal error will occur. If this were the case, gaze would miss the target location by a distance and direction equal to the vector of the stimulation-induced movement. Spatial models assume that the retinal error signal will be combined with information about the change in eye position produced by stimulation and predict that the animal will look to the position of the target in space. 2. Results confirm the predictions of spatial models. Animals compensated for the stimulation-induced perturbation by looking to the position of the target in space. The result predicted by retinocentric models-a saccade with a direction and amplitude based on retinal error alone-was never observed. 3. The eye movement that compensated for the change in eye position produced by stimulation was a saccade, not a passive, lowvelocity movement to an orbital position of mechanical equilibrium established by a tonic pattern of motoneuron activation specified by the visual target. This indicates that a new saccade command, based on stored information about the location of the retinal image and information about the new position of the eyes, had been issued. Computation of the vector of the compensatory saccade does not necessarily increase the latency of target acquisition. The interval between the end of a stimulation-induced saccade and the beginning of the compensatory saccade was frequently 20 ms or less, permitting the animal to acquire the target with a normal latency.

The basal ganglia have received a great deal of attention from modeling studies because of their putative role in normal motor function including action selection and sequencing, as well as their distubrances in Parkinson’s disease. However, their interaction is complex, and is thought to be more sophisticated than can be accounted for by simple box and plot diagrams. In the present study, we have examined trial by trial variations in response times in the stop signal task for both young (YA) and older (OA) adults. We compare previously reported YA data [1] with data collected from 18 older adults performing the same task. Unlike YA, the OA do not show a specific pattern of response times that is modulated by stop signal success in the previous trial. Additionally, the OA did not show an effect of inter trial interval (ITI) as was observed in YA. Based on our behavioral data [1], we concluded that a task switching interpretation was the most likely explanation of the YA results. We also compare the electrophysiological data collected during the ITI from OA and YA performing the stop signal task. In YA, the power spectral data revealed a midline frontal theta effect with more desynchronization following a stop signal trial. As in [1], we concluded that this evinced a task set switching interpretation as YA subjects went from a ‘ready to inhibit’ mode to a ‘ready to respond’ mode. In the OA data presented here, we failed to observe a similar frontal theta effect, which was expected given the lack of a behavioral result in the OA subjects. To test hypotheses about the role of the basal ganglia in task switching in young and older adults, we have developed a conductance-based network model of the subthalamic nucleus, internal and external segments of the globus pallidus. The model incorporates cellular properties described in previous modeling studies [3] based on experimental findings. First we establish network properties which lead to patterns of beta activity that are consistent with observed phenomenon in human subjects [2]. Next, we determine which network parameters affect trial to trial variations in response times within the model. Using this approach, we examine how known changes in healthy older adult basal ganglia may affect task performance. Similarly, we discuss the implications for Parkinson’s disease.

The intermediate layers of the superior colliculus (SC) contain neurons that clearly play a major role in regulating the production of saccadic eye movements: a burst of activity from saccade neurons (SNs) is thought to provide a drive signal to set the eyes in motion, whereas the tonic activity of fixation neurons (FNs) is thought to suppress saccades during fixation. The exact contribution of these neurons to saccade control is, however, unclear because the nature of the signals sent by the SC to the brain stem saccade generation circuit has not been studied in detail. Here we tested the hypothesis that the SC output signal is sufficient to control saccades by examining whether antidromically identified tectoreticular neurons (TRNs: 33 SNs and 13 FNs) determine the end of saccades. First, TRNs had discharge properties similar to those of nonidentified SC neurons and a proportion of output SNs had visually evoked responses, which signify that the saccade generator must receive and process visual information. Second, only a minority of TRNs possessed the temporal patterns of activity sufficient to terminate saccades: Output SNs did not cease discharging at the time of saccade end, possibly continuing to drive the brain stem during postsaccadic fixations, and output FNs did not resume their activity before saccade end. These results argue against a role for SC in regulating the timing of saccade termination by a temporal code and suggest that other saccade centers act to thwart the extraneous SC drive signal, unless it controls saccade termination by a spatial code.

Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses.

We investigated the link between neuronal activity in the frontal eye field (FEF) and the enhancement of visual processing associated with covert spatial attention in the absence of eye movements. We correlated activity recorded in the FEF of monkeys manually reporting the identity of a visual search target to performance accuracy and reaction time. Monkeys were cued to the most probable target location with a cue array containing a popout color singleton. Neurons exhibited spatially selective responses for the popout cue stimulus and for the target of the search array. The magnitude of activity related to the location of the cue prior to the presentation of the search array was correlated with trends in behavioral performance across valid, invalid, and neutral cue trial conditions. However, the speed and accuracy of the behavioral report on individual trials were predicted by the magnitude of spatial selectivity related to the target to be identified, not for the spatial cue. A minimum level of selectivity was necessary for target detection and a higher level for target identification. Muscimol inactivation of FEF produced spatially selective perceptual deficits in the covert search task that were correlated with the effectiveness of the inactivation and were strongest on invalid cue trials that require an endogenous attention shift. These results demonstrate a strong functional link between FEF activity and covert spatial attention and suggest that spatial signals from FEF directly influence visual processing during the time that a stimulus to be identified is being processed by the visual system.

Spatial attention is known to gate entry into visual short-term memory, and some evidence suggests that spatial signals may also play a role in binding features or protecting object representations during memory maintenance. To examine the persistence of spatial signals during object short-term memory, the activity of neurons in the Frontal Eye Field (FEF) of macaque monkeys was recorded during an object-based delayed match-to-sample (DMS) task. In this task monkeys were trained to remember an object image over a brief delay, irrespective of the locations of the sample or target presentation. FEF neurons exhibited visual, delay, and target period activity, including selectivity for sample location and target location. Delay period activity represented the sample location throughout the delay, despite the irrelevance of spatial information for successful task completion. Furthermore, neurons continued to encode sample position in a variant of the task in which the matching stimulus never appeared in their response field, confirming that FEF maintains sample location independent of subsequent behavioral relevance. FEF neurons also exhibited target-position-dependent anticipatory activity immediately prior to target onset, suggesting that monkeys predicted target position within blocks. These results show that FEF neurons maintain spatial information during short-term memory, even when that information is irrelevant for task performance.

Visually guided movements can be inaccurate, especially if unexpected events occur while the movement is programmed. Often errors of gaze are corrected before external feedback can be processed. Evidence is presented from macaque monkey frontal eye field (FEF), a cortical area that selects visual targets, allocates attention, and programs saccadic eye movements, for a neural mechanism that can correct saccade errors before visual afferent or performance monitoring signals can register the error. Macaques performed visual search for a color singleton that unpredictably changed position in a circular array as in classic double-step experiments. Consequently, some saccades were directed in error to the original target location. These were followed frequently by unrewarded, corrective saccades to the final target location. We previously showed that visually responsive neurons represent the new target location even if gaze shifted errantly to the original target location. Now we show that the latency of corrective saccades is predicted by the timing of movement-related activity in the FEF. Preceding rapid corrective saccades, the movement-related activity of all neurons began before explicit error signals arise in the medial frontal cortex. The movement-related activity of many neurons began before visual feedback of the error was registered and that of a few neurons began before the error saccade was completed. Thus movement-related activity leading to rapid corrective saccades can be guided by an internal representation of the environment updated with a forward model of the error.

Several decades of psychophysical and neurophysiological studies have established that visual signals are enhanced at the locus of attention. What remains a mystery is the mechanism that initiates biases in the strength of visual representations. Recent evidence argues that, during spatial attention, these biases reflect nascent saccadic eye movement commands. We examined the functional interaction of saccade preparation and visual coding by electrically stimulating sites within the frontal eye fields (FEF) and measuring its effect on the activity of neurons in extrastriate visual cortex. Here we show that visual responses in area V4 could be enhanced after brief stimulation of retinotopically corresponding sites within the FEF using currents below that needed to evoke saccades. The magnitude of the enhancement depended on the effectiveness of receptive field stimuli as well as on the presence of competing stimuli outside the receptive field. Stimulation of non-corresponding FEF representations could suppress V4 responses. The results suggest that the gain of visual signals is modified according to the strength of spatially corresponding eye movement commands.

1. We studied neuronal activity in the supplementary eye field (SEF) and frontal eye field (FEF) of a monkey during performance of a conditional motor task that required capturing of a target either with a saccadic eye movement (the saccade-only condition) or with an eye-hand reach (the saccade-and-reach condition), according to visual instructions. 2. Among 106 SEF neurons that showed presaccadic activity, more than one-half of them (54%) were active preferentially under the saccade-only condition (n = 12) or under the saccade-and-reach condition (n = 45), while the remaining 49 neurons were equally active in both conditions. 3. By contrast, most (97%) of the 109 neurons in the FEF exhibited approximately equal activity in relation to saccades under the two conditions. 4. The present results suggest the possibility that SEF neurons, at least in part, are involved in signaling whether the motor task is oculomotor or combined eye-arm movements, whereas FEF neurons are mostly related to oculomotor control.

1. We studied neuronal activity in the monkey's frontal eye field (FEF) in conjunction with saccades directed to auditory targets. 2. All FEF neurons with movement activity preceding saccades to visual targets also were active preceding saccades to auditory targets, even when such saccades were made in the dark. Movement cells generally had comparable bursts for aurally and visually guided saccades; visuomovement cells often had weaker bursts in conjunction with aurally guided saccades. 3. When these cells were tested from different initial fixation directions, movement fields associated with aurally guided saccades, like fields mapped with visual targets, were a function of saccade dimensions, and not the speaker's spatial location. Thus, even though sound location cues are chiefly craniotopic, the crucial factor for a FEF discharge before aurally guided saccades was the location of auditory target relative to the current direction of gaze. 4. Intracortical microstimulation at the sites of these cells evoked constant-vector saccades, and not goal-directed saccades. The direction and size of electrically elicited saccades generally matched the cell's movement field for aurally guided saccades. 5. Thus FEF activity appears to have a role in aurally guided as well as visually guided saccades. Moreover, visual and auditory target representations, although initially obtained in different coordinate systems, appear to converge to a common movement vector representation at the FEF stage of saccadic processing that is appropriate for transmittal to saccade-related burst neurons in the superior colliculus and pons.

An internal model for predictive saccades in frontal cortex was investigated by recording neurons in monkey frontal eye field during an inferred motion task. Monkeys were trained to make saccades to the extrapolated position of a small moving target that was rendered temporarily invisible and whose trajectory was altered. On roughly two-thirds of the trials, monkeys made multiple saccades while the target was invisible. Primary saccades were correlated with extrapolated target position. Secondary saccades significantly reduced residual errors resulting from imperfect accuracy of the first saccade. These observations suggest that the second saccade was corrective. As there was no visual feedback, corrective saccades could only be driven by an internally generated error signal. Neuronal activity in the frontal eye field was directionally tuned prior to both primary and secondary saccades. Separate subpopulations of cells encoded either saccade direction or direction error prior to the second saccade. These results suggest that FEF neurons encode the error after the first saccade, as well as the direction of the second saccade. Hence, FEF appears to contribute to detecting and correcting movement errors based on internally generated signals.

Particle loading as a design parameter for composite radiation shielding

Context Strategies for achieving greater ruminant livestock productivity are essential to meet the food demands of growing populations, but sustainable changes are difficult to identify given the inherent complexity of such systems. Systems models can address this issue by allowing the impact of potential changes to be explored. Aims To develop a holistic systems model for goat production in an extensive Mediterranean environment which could allow changes in key management factors influencing the system to be investigated. Methods Initially, a conceptual comprehensive stock-and-flow model of a representative Mediterranean goat production system was constructed. This was used to identify informative indicators that would represent the overall technical and economic performance of the system. Sub-models were then assembled to build the full systems model. The model was parameterised with data collected over 3 years for goat holdings in northern Morocco. Scenario analysis techniques are used to explore the strategies that optimise performance under climate and feed price challenges. Key results Meat production is particularly important during periods of drought when increased meat yields can counteract the expected reduction in milk yields, to protect human food security, prevent excessive rangeland degradation and preserve natural nutritional resources. Feed price shocks during drought can have significant negative impacts on the system and zero feed input is shown to be a more sustainable strategy than reliance on high price feed during drought. Any alternative feed sources need to have a high forage component to reduce grazing periods significantly and promote rangeland preservation. Implications A diverse management strategy with a mixed meat and dairy semi-intensive production is more stable than specialised dairy systems and allows goat production and financial viability of intensification to be maintained under climatic stress; maintaining meat production was necessary to optimise performance. Conclusions The model allows improved insight into management strategies which could optimise animal husbandry performance in goat subsistence systems. However, the work also demonstrates the difficulty of constructing a truly holistic model since, to be practical, such constructs must necessarily be bounded; parameter selection and the limits to the boundaries imposed are inevitably critical.

Sequences of saccadic eye movements are instrumental in navigating our visual environment. While neural activity has been shown to ramp up to a threshold before single saccades, the neural underpinnings of multiple saccades is unknown. To understand the neural control of saccade sequences, we recorded from the frontal eye field (FEF) of macaque monkeys while they performed a sequential saccade task. We show that the concurrent planning of two saccade plans brings forth processing bottlenecks, specifically by decreasing the growth rate and increasing the threshold of saccade-related ramping activity. The rate disruption affected both saccade plans, and a computational model, wherein activity related to the two saccade plans mutually and asymmetrically inhibited each other, predicted the behavioral and neural results observed experimentally. Borrowing from models in psychology, our results demonstrate a capacity-sharing mechanism of processing bottlenecks, wherein multiple saccade plans in a sequence compete for the processing capacity by the perturbation of the saccade-related ramping activity. Finally, we show that, in contrast to movement-related neurons, visual activity in FEF neurons is not affected by the presence of multiple saccade targets, indicating that, for perceptually simple tasks, inhibition within movement-related neurons mainly instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.