Jeffrey D. Schall

Neural Control of Voluntary Movement Initiation

When humans respond to sensory stimulation, their reaction times tend to be long and variable relative to neural transduction and transmission times. The neural processes responsible for the duration and variability of reaction times are not understood. Single-cell recordings in a motor area of the cerebral cortex in behaving rhesus monkeys (Macaca mulatta) were used to evaluate two alternative mathematical models of the processes that underlie reaction times. Movements were initiated if and only if the neural activity reached a specific and constant threshold activation level. Stochastic variability in the rate at which neural activity grew toward that threshold resulted in the distribution of reaction times. This finding elucidates a specific link between motor behavior and activation of neurons in the cerebral cortex.

NEURAL BASIS OF DECIDING, CHOOSING AND ACTING

The ability and opportunity to make decisions and carry out effective actions in pursuit of goals is central to intelligent life. Recent research has provided significant new insights into how the brain arrives at decisions, makes choices, and produces and evaluates the consequences of actions. In fact, by monitoring or manipulating specific neurons, certain choices can now be predicted or manipulated.

Performance monitoring by the supplementary eye field

Intelligent behaviour requires self-control based on the consequences of actions. The countermanding task is designed to study self-control; it requires subjects to withhold planned movements in response to an imperative stop signal, which they can do with varying success. In humans, the medial frontal cortex has been implicated in the supervisory control of action. In monkeys, the supplementary eye field in the dorsomedial frontal cortex is involved in producing eye movements, but its precise function has not been clarified. To investigate the role of the supplementary eye field in the control of eye movements, we recorded neural activity in macaque monkeys trained to perform an eye movement countermanding task. Distinct groups of neurons were active after errors, after successful withholding of a partially prepared movement, or in association with reinforcement. These three forms of activation could not be explained by sensory or motor factors. Our results lead us to put forward the hypothesis that the supplementary eye field contributes to monitoring the context and consequences of eye movements.

Inhibitory control in mind and brain: An interactive race model of countermanding saccades

The stop-signal task has been used to study normal cognitive control and clinical dysfunction. Its utility is derived from a race model that accounts for performance and provides an estimate of the time it takes to stop a movement. This model posits a race between go and stop processes with stochastically independent finish times. However, neurophysiological studies demonstrate that the neural correlates of the go and stop processes produce movements through a network of interacting neurons. The juxtaposition of the computational model with the neural data exposes a paradox-how can a network of interacting units produce behavior that appears to be the outcome of an independent race? The authors report how a simple, competitive network can solve this paradox and provide an account of what is measured by stop-signal reaction time.

Effects of similarity and history on neural mechanisms of visual selection

To investigate how the brain combines knowledge with visual processing to locate eye movement targets, we trained monkeys to search for a target defined by a conjunction of color and shape. On successful trials, neurons in the frontal eye field not only discriminated the target from distractors, but also discriminated distractors that shared a target feature as well as distractors that had been the search target during the previous session. Likewise, occasional errant saccades tended to direct gaze to distractors that either resembled the current target or had been the previous target. These findings show that the frontal eye field is involved in visual and not just motor selection and that visual selection is influenced by long-term priming. The data support the hypothesis that visual selection can be accomplished by parallel processing of objects based on their elementary features.

Monitoring and Control of Action by the Frontal Lobes

Success requires deciding among alternatives, controlling the initiation of movements, and judging the consequences of actions. When alternatives are difficult to distinguish, habitual responses must be overcome, or consequences are uncertain, deliberation is necessary and a supervisory system exerts control over the processes that produce sensory-guided movements. We have investigated these processes by recording neural activity in the frontal lobe of macaque monkeys performing a countermanding task. Distinct neurons in the frontal eye field respond to visual stimuli or control the production of the movements. In the supplementary eye field and anterior cingulate cortex, neurons appear not to control directly movement initiation but instead signal the production of errors, the anticipation and delivery of reinforcement, and the presence of processing conflict. These signals form the core of current models of supervisory control of sensorimotor processes.

Effects of Stimulus-Response Compatibility on Neural Selection in Frontal Eye Field

We investigated the neural basis of visual and saccade selection in the frontal eye field of macaque monkeys using a singleton search task with prosaccade or antisaccade responses. Two types of neurons were distinguished. The first initially selected the singleton even in antisaccade trials, although most subsequently selected the endpoint of the saccade. The time the singleton was located was not affected by stimulus-response compatibility and did not vary with reaction time across trials. The second type of neuron selected only the endpoint of the saccade. The time of endpoint selection by these neurons accounted for most of the effect of stimulus-response compatibility on reaction time. These results indicate that visual selection and saccade selection are different processes.

Neurally constrained modeling of perceptual decision making.

Stochastic accumulator models account for response time in perceptual decision-making tasks by assuming that perceptual evidence accumulates to a threshold. The present investigation mapped the firing rate of frontal eye field (FEF) visual neurons onto perceptual evidence and the firing rate of FEF movement neurons onto evidence accumulation to test alternative models of how evidence is combined in the accumulation process. The models were evaluated on their ability to predict both response time distributions and movement neuron activity observed in monkeys performing a visual search task. Models that assume gating of perceptual evidence to the accumulating units provide the best account of both behavioral and neural data. These results identify discrete stages of processing with anatomically distinct neural populations and rule out several alternative architectures. The results also illustrate the use of neurophysiological data as a model selection tool and establish a novel framework to bridge computational and neural levels of explanation.

On the role of frontal eye field in guiding attention and saccades

The neural bases of shifting attention and directing gaze were investigated in macaque monkeys performing a singleton search that required a prosaccade, antisaccade, or no saccade cued by the shape of the singleton. In prosaccade trials, most neurons in frontal eye field selected the location of the singleton that was also the end point of the saccade. In antisaccade trials, most neurons selected the singleton followed by selection of the endpoint of the saccade. Other neurons selected only the endpoint of the saccade in antisaccade trials. When no saccade was produced, many of the first type of neuron still selected the singleton, and many but not all of both types of neurons later selected the stimulus opposite the singleton even though no saccade was produced. These patterns of activity are consistent with the hypotheses that covert shifts of attention can occur without saccade production and that FEF contributes to covert as well as overt orienting.

Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis

The purpose of this study was to investigate the temporal relationship between presaccadic neuronal discharges in the frontal eye fields (FEF) and supplementary eye fields (SEF) and the initiation of saccadic eye movements in macaque. We utilized an analytical technique that could reliably identify periods of neuronal modulation in individual spike trains. By comparing the observed activity of neurons with the random Poisson distribution generated from the mean discharge rate during the trial period, the period during which neural activity was significantly elevated with a predetermined confidence level was identified in each spike train. In certain neurons, bursts of action potentials were identified by determining the period in each spike train in which the activation deviated most from the expected Poisson distribution. Using this method, we related these defined periods of modulation to saccade initiation in specific cell types recorded in FEF and SEF. Cells were recorded in SEF while monkeys made saccades to targets presented alone. Cells were recorded in FEF while monkeys made saccades to targets presented alone or with surrounding distractors. There were no significant differences in the time-course of activity of the population of FEF presaccadic movement cells prior to saccades generated to singly presented or distractor-embedded targets. The discharge of presaccadic movement cells in FEF and SEF could be subdivided quantitatively into an early prelude followed by a high-rate burst of activity that occurred at a consistent interval before saccade initiation. The time of burst onset relative to saccade onset in SEF presaccadic movement cells was earlier and more variable than in FEF presaccadic movement cells. The termination of activity of another population of SEF neurons, known as preparatory set cells, was time-locked to saccade initiation. In addition, the cessation of SEF preparatory set cell activity coincided precisely with the beginning of the burst of SEF presaccadic movement cells. This finding raises the possibility that SEF preparatory set cells may be involved in saccade initiation by regulating the activation of SEF presaccadic movement cells. These results demonstrate the utility of the Poisson spike train analysis to relate periods of neuronal modulation to behavior.