Mark A. Segraves

Visuospatial and motor attention in the monkey

Visuospatial attention involves the selection of stimuli from the environment for further neural processing. The attention-related enhancement of visual responses in posterior parietal cortex is a possible neural substrate for visuospatial attention. By analogy with the selection process in the spatial domain, motor attention is postulated to involve a selection among simultaneous upper motor signals. Selection of motor programs within the oculomotor system is used as an example of this attentional process. Since attentive fixation modulates the effect on the oculomotor system of electrical stimulation of the frontal eye fields, a given upper motor neuronal signal need not necessarily invoke a movement. That the brain has multiple simultaneous motor signals is apparent from the profusion of sensory-driven upper motor neurons. The frontal cortex is probably important in selecting which upper motor signals actually evoke movements, by elaborating motor programs for purposive behavior, but not for all movements.

Predictive Activity in Macaque Frontal Eye Field Neurons During Natural Scene Searching

Generating sequences of multiple saccadic eye movements allows us to search our environment quickly and efficiently. Although the frontal eye field cortex (FEF) has been linked to target selection and making saccades, little is known about its role in the control and performance of the sequences of saccades made during self-guided visual search. We recorded from FEF cells while monkeys searched for a target embedded in natural scenes and examined the degree to which cells with visual and visuo-movement activity showed evidence of target selection for future saccades. We found that for about half of these cells, activity during the fixation period between saccades predicted the next saccade in a sequence at an early time that precluded selection based on current visual input to a cells response field. In addition to predicting the next saccade, activity during the fixation prior to two successive saccades also predicted the direction and goal of the second saccade in the sequence. We refer to this as advanced predictive activity. Unlike activity indicating the upcoming saccade, advanced predictive activity occurred later in the fixation period, mirroring the order of the saccade sequence itself. The remaining cells without advanced predictive activity did not predict future saccades but reintroduced the signal for the upcoming saccade at an intermediate time in the fixation period. Together these findings suggest that during natural visual search the timing of FEF cell activity is consistent with a role in specifying targets for one or more future saccades in a search sequence.

Effect of stimulus position and velocity upon the maintenance of smooth pursuit eye velocity

The relative contributions of retinal slip velocity and position errors to the generation of smooth pursuit eye movements were examined in three rhesus monkeys. Recognizing the unlikelihood of producing a pure retinal slip velocity or position error signal, these two stimulus parameters were combined under open-loop conditions. Both slip velocity and position error were used by the monkey to maintain an established eye velocity. Both parameters had the greatest effects upon eye velocity when they were in the same direction, enabling the monkey to maintain an established pursuit velocity. When slip velocity and position error were in the direction opposite to the initial pursuit, eye velocity reversed direction and moved very quickly towards zero. When the two parameters were in opposite directions, their effect upon eye velocity was minimized.

Saliency and Saccade Encoding in the Frontal Eye Field During Natural Scene Search

The frontal eye field (FEF) plays a central role in saccade selection and execution. Using artificial stimuli, many studies have shown that the activity of neurons in the FEF is affected by both visually salient stimuli in a neurons receptive field and upcoming saccades in a certain direction. However, the extent to which visual and motor information is represented in the FEF in the context of the cluttered natural scenes we encounter during everyday life has not been explored. Here, we model the activities of neurons in the FEF, recorded while monkeys were searching natural scenes, using both visual and saccade information. We compare the contribution of bottom-up visual saliency (based on low-level features such as brightness, orientation, and color) and saccade direction. We find that, while saliency is correlated with the activities of some neurons, this relationship is ultimately driven by activities related to movement. Although bottom-up visual saliency contributes to the choice of saccade targets, it does not appear that FEF neurons actively encode the kind of saliency posited by popular saliency map theories. Instead, our results emphasize the FEFs role in the stages of saccade planning directly related to movement generation.

Single trial-based prediction of a go/no-go decision in monkey superior colliculus

While some decision-making processes often result in the generation of an observable action, for example eye or limb movements, others may prevent actions and occur without an overt behavioral response. To understand how these decisions are made, one must look directly at their neuronal substrates. We trained two monkeys on a go/no-go task which requires a saccade to a peripheral cue stimulus (go) or maintenance of fixation (no-go). We performed binary regressions on the activity of single neurons in the superior colliculus (SC), with the go/no-go decision as a predictor variable, and constructed a virtual decision function (VDF) designed to provide a good estimation of decision content and its timing in a single trial decision process. Post hoc analyses by VDF correctly predicted the monkeys choice in more than 80% of trials. These results suggest that monitoring of SC activity has sufficient capacity to predict go/no-go decisions on a trial-by-trial basis.

Inhibition in superior colliculus neurons in a brightness discrimination task

Simultaneous recordings were collected from between two and four buildup neurons from the left and right superior colliculi in rhesus monkeys in a simple two-choice brightness discrimination task. The monkeys were required to move their eyes to one of two response targets to indicate their decision. Neurons were identified whose receptive fields were centered on the response targets. The functional role of inhibition was examined by conditionalizing firing rate on a high versus low rate in target neurons 90 ms to 30 ms before the saccade and examining the firing rate in both contralateral and ipsilateral neurons. Two models with racing diffusion processes were fit to the behavioral data, and the same analysis was performed on simulated paths in the diffusion processes that have been found to represent firing rate. The results produce converging evidence for the lack of a functional role for inhibition between neural populations corresponding to the two decisions.

A pressure system for the microinjection of substances into the brain of awake monkeys

We describe a method for placing pressure microinjections of drugs or anatomical tracers in physiologically defined sites in the brain of awake monkeys. This method provides a means to record neuronal activity from the tip of an injection cannula so that an injection can be made at a physiologically defined location. It uses pressure in a closed system to precisely control the amount of fluid injected and provides a visible means for monitoring injection volume. The injection cannula is easy to make with readily available components and can be used repeatedly for multiple recording sessions and injections.

Visual Experience Is Required for the Development of Eye Movement Maps in the Mouse Superior Colliculus

Topographic maps are a fundamental feature of the brains representations of the sensory environment as well as an efficient way to organize motor control networks. Although great progress has been made in our understanding of sensory map development, very little is known about how topographic representations for motor control develop and interface with sensory maps. Here we map the representation for eye movements in the superior colliculus (SC) in awake mice. As stimulation sites were sampled along the anterior–posterior axis, small amplitude, nasally directed (ipsiversive) saccadic eye movements were evoked by microstimulation in anterior SC, followed by a smooth progression to large, temporally directed (contraversive) movements in posterior SC. This progressive change of movement amplitude and direction is consistent with the global polarity of the retinotopic map in the superficial SC, just as in primates and cats. We then investigated the role of visual experience in the development of eye movement map by studying mice reared in complete darkness. Saccades evoked by SC stimulation as well as spontaneous saccadic eye movements were larger in the dark-reared mice, indicating that visual experience is required to fine-tune the gain of saccades and to establish normal eye movement maps in the SC. Our experiments provide a foundation for future studies to investigate the synaptic organization and developmental mechanisms of sensorimotor transformations in mice. SIGNIFICANCE STATEMENT The superior colliculus (SC) is a midbrain structure important for multisensory integration and sensorimotor transformation. Here we have studied eye movement representations in the SC of mice, a species that has become a popular model in vision research because of available genetic tools. Our studies show mice make saccadic eye movements spontaneously and in response to SC stimulation. The mouse SC contains an eye movement map that has the same global polarity as the overlaying visual map, just like in cats and primates. Furthermore, we show that visual experience is required for establishing the normal eye movement map. Our study provides a necessary basis for future mechanistic studies of how SC motor maps develop and become aligned with sensory maps.

2009 Special Issue: Neural mind reading of multi-dimensional decisions by monkey mid-brain activity

Brain-machine interfaces (BMIs) have the potential to improve the quality of life for individuals with disabilities. We engaged in the development of neural mind-reading techniques for cognitive BMIs to provide a readout of decision processes. We trained 2 monkeys on go/no-go tasks, and monitored the activity of groups of neurons in their mid-brain superior colliculus (SC). We designed a virtual decision function (VDF) reflecting the continuous progress of binary decisions on a single-trial basis, and applied it to the ensemble activity of SC neurons. Post hoc analyses using the VDF predicted the cue location as well as the monkeys motor choice (go or no-go) soon after the presentation of the cue. These results suggest that our neural mind-reading techniques have the potential to provide rapid real-time control of communication support devices.

Feature-based attention and spatial selection in frontal eye fields during natural scene search

When we search for visual objects, the features of those objects bias our attention across the visual landscape (feature-based attention). The brain uses these top-down cues to select eye movement targets (spatial selection). The frontal eye field (FEF) is a prefrontal brain region implicated in selecting eye movements and is thought to reflect feature-based attention and spatial selection. Here, we study how FEF facilitates attention and selection in complex natural scenes. We ask whether FEF neurons facilitate feature-based attention by representing search-relevant visual features or whether they are primarily involved in selecting eye movement targets in space. We show that search-relevant visual features are weakly predictive of gaze in natural scenes and additionally have no significant influence on FEF activity. Instead, FEF activity appears to primarily correlate with the direction of the upcoming eye movement. Our result demonstrates a concrete need for better models of natural scene search and suggests that FEF activity during natural scene search is explained primarily by spatial selection.