Variable Statistical Structure of Neuronal Spike Trains in Monkey Superior Colliculus.

Popular models of decision-making propose that noisy sensory evidence accumulates until reaching a bound. Behavioral evidence as well as trial-averaged ramping of neuronal activity in sensorimotor regions of the brain support this idea. However, averaging activity across trials can mask other processes, such as rapid shifts in decision commitment, calling into question the hypothesis that evidence accumulation is encoded by delay period activity of individual neurons. We mined two sets of data from experiments in four monkeys in which we recorded from superior colliculus neurons during two different decision-making tasks and a delayed saccade task. We applied second-order statistical measures and spike train simulations to determine whether spiking statistics were similar or different in the different tasks and monkeys, despite similar trial-averaged activity across tasks and monkeys. During a motion direction discrimination task, single-trial delay period activity behaved statistically consistent with accumulation. During an orientation detection task, the activity behaved superficially like accumulation, but statistically consistent with stepping. Simulations confirmed both findings. Importantly, during a simple saccade task, with similar trial-averaged activity, neither process explained spiking activity, ruling out interpretations based on differences in attention, reward, or motor planning. These results highlight the need for exploring single-trial spiking dynamics to understand cognitive processing and raise the interesting hypothesis that the superior colliculus participates in different aspects of decision-making depending on task differences.SIGNIFICANCE STATEMENT How are decisions based on sensory information transformed into actions? We report that single-trial neuronal activity dynamics in the superior colliculus of monkeys show differences in decision-making tasks depending on task idiosyncrasies and requirements and despite similar trial-averaged ramping activity. These results highlight the importance of exploring single-trial spiking dynamics to understand cognitive processing and raise the interesting hypothesis that the superior colliculus participates in different aspects of decision-making depending on task requirements.

A Role for the Superior Colliculus in Decision Criteria.

Simple decisions arise from the evaluation of sensory evidence. But decisions are determined by more than just evidence. Individuals establish internal decision criteria that influence how they respond. Where or how decision criteria are established in the brain remains poorly understood. Here, we show that neuronal activity in the superior colliculus (SC) predicts changes in decision criteria. Using a novel "Yes-No" task that isolates changes in decision criterion from changes in decision sensitivity, and computing neuronal measures of sensitivity and criterion, we find that SC neuronal activity correlates with the decision criterion regardless of the location of the choice report. We also show that electrical manipulation of activity within the SC produces changes in decisions consistent with changes in decision criteria and are largely independent of the choice report location. Our correlational and causal results together provide strong evidence that SC activity signals the position of a decision criterion. VIDEO ABSTRACT.

The effect of face patch microstimulation on perception of faces and objects.

What is the range of stimuli encoded by face-selective regions of the brain? We asked how electrical microstimulation of face patches in macaque inferotemporal cortex affects perception of faces and objects. We found that microstimulation strongly distorted face percepts and that this effect depended on precise targeting to the center of face patches. While microstimulation had no effect on the percept of many non-face objects, it did affect the percept of some, including non-face objects whose shape is consistent with a face (for example, apples) as well as somewhat facelike abstract images (for example, cartoon houses). Microstimulation even perturbed the percept of certain objects that did not activate the stimulated face patch at all. Overall, these results indicate that representation of facial identity is localized to face patches, but activity in these patches can also affect perception of face-compatible non-face objects, including objects normally represented in other parts of inferotemporal cortex.

Insights into decision making using choice probability.

A long-standing question in systems neuroscience is how the activity of single neurons gives rise to our perceptions and actions. Critical insights into this question occurred in the last part of the 20th century when scientists began linking modulations of neuronal activity directly to perceptual behavior. A significant conceptual advance was the application of signal detection theory to both neuronal activity and behavior, providing a quantitative assessment of the relationship between brain and behavior. One metric that emerged from these efforts was choice probability (CP), which provides information about how well an ideal observer can predict the choice an animal makes from a neuron's discharge rate distribution. In this review, we describe where CP has been studied, locational trends in the values found, and why CP values are typically so low. We discuss its dependence on correlated activity among neurons of a population, assess whether it arises from feedforward or feedback mechanisms, and investigate what CP tells us about how many neurons are required for a decision and how they are pooled to do so.

Frontal eye field neurons assess visual stability across saccades.

The image on the retina may move because the eyes move, or because something in the visual scene moves. The brain is not fooled by this ambiguity. Even as we make saccades, we are able to detect whether visual objects remain stable or move. Here we test whether this ability to assess visual stability across saccades is present at the single-neuron level in the frontal eye field (FEF), an area that receives both visual input and information about imminent saccades. Our hypothesis was that neurons in the FEF report whether a visual stimulus remains stable or moves as a saccade is made. Monkeys made saccades in the presence of a visual stimulus outside of the receptive field. In some trials, the stimulus remained stable, but in other trials, it moved during the saccade. In every trial, the stimulus occupied the center of the receptive field after the saccade, thus evoking a reafferent visual response. We found that many FEF neurons signaled, in the strength and timing of their reafferent response, whether the stimulus had remained stable or moved. Reafferent responses were tuned for the amount of stimulus translation, and, in accordance with human psychophysics, tuning was better (more prevalent, stronger, and quicker) for stimuli that moved perpendicular, rather than parallel, to the saccade. Tuning was sometimes present as well for nonspatial transaccadic changes (in color, size, or both). Our results indicate that FEF neurons evaluate visual stability during saccades and may be general purpose detectors of transaccadic visual change.

Frontal eye field neurons with spatial representations predicted by their subcortical input.

The frontal eye field (FEF) is a cortical structure involved in cognitive aspects of eye movement control. Neurons in the FEF, as in most of cerebral cortex, primarily represent contralateral space. They fire for visual stimuli in the contralateral field and for saccadic eye movements made to those stimuli. Yet many FEF neurons engage in sophisticated functions that require flexible spatial representations such as shifting receptive fields and vector subtraction. Such functions require knowledge about all of space, including the ipsilateral hemifield. How does the FEF gain access to ipsilateral information? Here, we provide evidence that one source of ipsilateral information may be the opposite superior colliculus (SC) in the midbrain. We physiologically identified neurons in the FEF that receive input from the opposite SC, same-side SC, or both. We found a striking structure-function relationship: the laterality of the response field of an FEF neuron was predicted by the laterality of its SC inputs. FEF neurons with input from the opposite SC had ipsilateral fields, whereas neurons with input from the same-side SC had contralateral fields. FEF neurons with input from both SCs had lateralized fields that could point in any direction. The results suggest that signals from the two SCs provide each FEF with information about all of visual space, a prerequisite for higher level sensorimotor computations.

Corollary discharge circuits in the primate brain.

Movements are necessary to engage the world, but every movement results in sensorimotor ambiguity. Self-movements cause changes to sensory inflow as well as changes in the positions of objects relative to motor effectors (eyes and limbs). Hence the brain needs to monitor self-movements, and one way this is accomplished is by routing copies of movement commands to appropriate structures. These signals, known as corollary discharge (CD), enable compensation for sensory consequences of movement and preemptive updating of spatial representations. Such operations occur with a speed and accuracy that implies a reliance on prediction. Here we review recent CD studies and find that they arrive at a shared conclusion: CD contributes to prediction for the sake of sensorimotor harmony.

The frontal eye field as a prediction map.

Predictive processes are widespread in the motor and sensory areas of the primate brain. They enable rapid computations despite processing delays and assist in resolving noisy, ambiguous input. Here we propose that the frontal eye field, a cortical area devoted to sensorimotor aspects of eye movement control, implements a prediction map of the postsaccadic visual scene for the purpose of constructing a stable percept despite saccadic eye movements.

Corollary discharge across the animal kingdom.

Our movements can hinder our ability to sense the world. Movements can induce sensory input (for example, when you hit something) that is indistinguishable from the input that is caused by external agents (for example, when something hits you). It is critical for nervous systems to be able to differentiate between these two scenarios. A ubiquitous strategy is to route copies of movement commands to sensory structures. These signals, which are referred to as corollary discharge (CD), influence sensory processing in myriad ways. Here we review the CD circuits that have been uncovered by neurophysiological studies and suggest a functional taxonomic classification of CD across the animal kingdom. This broad understanding of CD circuits lays the groundwork for more challenging studies that combine neurophysiology and psychophysics to probe the role of CD in perception.