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Neural circuits that translate sensory information into motor commands are organized in a feedforward manner converting sensory information into motor output. The superior colliculus (SC) follows this pattern as it plays a role in converting visual information from the retina and visual cortex into motor commands for rapid eye movements (saccades). Feedback from movement to sensory regions is hypothesized to play critical roles in attention, visual image stability, and saccadic suppression, but in contrast to feedforward pathways, motor feedback to sensory regions has received much less attention. The present study used voltage imaging and patch-clamp recording in slices of rat SC to test the hypothesis of an excitatory synaptic pathway from the motor layers of the SC back to the sensory superficial layers. Voltage imaging revealed an extensive depolarization of the superficial layers evoked by electrical stimulation of the motor layers. A pharmacologically isolated excitatory synaptic potential in the superficial layers depended on stimulus strength in the motor layers in a manner consistent with orthodromic excitation. Patch-clamp recording from neurons in the sensory layers revealed excitatory synaptic potentials in response to glutamate application in the motor layers. The location, size, and morphology of responsive neurons indicated they were likely to be narrow-field vertical cells. This excitatory projection from motor to sensory layers adds an important element to the circuitry of the SC and reveals a novel feedback pathway that could play a role in enhancing sensory responses to attended targets as well as visual image stabilization.

Brain regions involved in transforming sensory signals into movement commands are the likely sites where decisions are formed. Once formed, a decision must be read out from the activity of populations of neurons to produce a choice of action. How this occurs remains unresolved. We recorded from four superior colliculus neurons simultaneously while monkeys performed a target selection task. We implemented three models to gain insight into the computational principles underlying population coding of action selection. We compared the population vector average (PVA)/optimal linear estimator (OLE) and winner-takes-all (WTA) models and a Bayesian model, maximum a posteriori estimate (MAP), to determine which predicted choices most often. The probabilistic model predicted more trials correctly than both the WTA and the PVA. The MAP model predicted 81.88%, whereas WTA predicted 71.11% and PVA/OLE predicted the least number of trials at 55.71 and 69.47%. Recovering MAP estimates using simulated, nonuniform priors that correlated with monkeys' choice performance, improved the accuracy of the model by 2.88%. A dynamic analysis revealed that the MAP estimate evolved over time and the posterior probability of the saccade choice reached a maximum at the time of the saccade. MAP estimates also scaled with choice performance accuracy. Although there was overlap in the prediction abilities of all the models, we conclude that movement choice from populations of neurons may be best understood by considering frameworks based on probability.

How the brain selects goals for movements remains unknown. The system designed to move the eyes rapidly, the saccadic system, may play a role. Here we ask how sensory signals within a saccade area are influenced by selecting and preparing a saccade. Trained monkeys made or withheld saccades, based on a color cue, to targets varying in luminance contrast. We measured the initial visual activity of superior colliculus (SC) neurons in response to the appearance of these targets. We determined neuronal contrast responses in three task conditions: when two luminance gratings appeared one in the response field (RF) and one in the mirror-opposite location and a cue to select the stimulus in the RF occurred; when the gratings appeared and a cue to select the stimulus out of the RF occurred; and third, when the gratings appeared but monkeys remained fixating on the central spot. SC neurons had increases in visual responses when contrast increased. Receiver operating characteristic analysis revealed an increased ability of neurons to detect the grating on trials with higher contrast targets and also on trials with a cue to make a saccade compared with trials with a cue to remain fixating. Using two measures of neuronal sensitivity, those SC neurons considered part of the motor circuitry increased their sensitivity to contrast with a cue to make a saccade. The results indicate that movement commands influence sensory responses in SC in much the same way that commands to shift attention influence sensory responses in extrastriate cortex.

How the brain selects one action from among multiple options is unknown. A main tenet of signal detection theory (SDT) is that sensory stimuli are represented as noisy information channels. Therefore, the accuracy of selection might be predicted by how well neuronal activity representing alternatives can be distinguished. Here, we apply an SDT framework to a motor system by recording from superior colliculus (SC) neurons during performance of a color, oddball selection task. We recorded from sets of four neurons simultaneously, each of the four representing one of the four possible targets. Because the electrode placement constrained the position of the stimuli in the visual field, the stimulus arrangement varied across experiments. This variability in stimulus arrangement led to variability in choices allowing us to explore the relationship between SC neuronal activity and performance accuracy. SC target neurons had higher levels of discharge than SC distractor neurons in subsets of trials when selection performance was very accurate. In subsets of trials when performance was poor, the discharge level decreased in target neurons and increased in distractor neurons. Accurate performance was associated with larger separations between neuronal activity from targets and distractors as quantified by the receiver operating characteristic (ROC) area andd′(an index of discriminability). Poorer performance was associated with less separation of target and distractor neuronal activity. ROC area andd′scaled approximately linearly with performance accuracy. Furthermore, ROC area andd′increased as saccade onset approached. Together, the results indicate that SC buildup neuronal activity signals the saccadic eye movement decision.

In addition to its role in saccade generation, the superior colliculus (SC) is involved in target selection, saccade selection, and shifting the focus of spatial attention. Here, we investigated the influence of saccade selection on sensory interactions within single response fields (RFs) of SC neurons. One or two differently shaped stimuli were presented within single RFs of SC neurons, and the shape of a centrally located cue indicated whether and where to make a saccade (Go-Go) or whether to make or withhold a saccade (Go/No-Go). We found that, when two stimuli appeared at different locations within a single RF, SC neuronal activity was reduced compared with when a single stimulus appeared in isolation within the center of the RF in both the Go-Go and Go/No-Go tasks. In both tasks, a subsequent cue indicating one stimulus as a saccade target reduced the influence of the second stimulus located within the RF. We found that the time course of the suppression resulting from the two stimuli was ∼130 ms, a time close to that seen in cortex. Finally, we found that the influence of two stimuli within single RFs of SC neurons changed over time in both the Go-Go and the Go/No-Go tasks. Initially, the neurons averaged the influence of two stimuli. As the trial progressed, the SC neurons signaled only the saccade vector that was produced. We conclude that cues to shift gaze, like attention, modulate the influence of sensory interactions, providing additional support for the linkage between attention and saccade selection.

Hyperexcitable reflex blinks are a cardinal sign of Parkinson’s disease. We investigated the neural circuit through which a loss of dopamine in the substantia nigra pars compacta (SNc) leads to increased reflex blink excitability. Through its inhibitory inputs to the thalamus, the basal ganglia could modulate the brainstem reflex blink circuits via descending cortical projections. Alternatively, with its inhibitory input to the superior colliculus, the basal ganglia could regulate brainstem reflex blink circuits via tecto-reticular projections. Our study demonstrated that the basal ganglia utilizes its GABAergic input to the superior colliculus to modulate reflex blinks. In rats with previous unilateral 6-hydroxydopamine (6-OHDA) lesions of the dopamine neurons of the SNc, we found that microinjections of bicuculline, a GABA antagonist, into the superior colliculus of both alert and anesthetized ratseliminatedthe reflex blink hyperexcitability associated with dopamine depletion. In normal, alert rats, decreasing the basal ganglia output to the superior colliculus by injecting muscimol, a GABA agonist, into the substantia nigra pars reticulata (SNr) markedlyreducedblink amplitude. Finally, brief trains of microstimulation to the superior colliculusreducedblink amplitude. Histological analysis revealed that effective muscimol microinjection and microstimulation sites in the superior colliculus overlapped the nigro-tectal projection from the basal ganglia. These data support models of Parkinsonian symtomatology that rely on changes in the inhibitory drive from basal ganglia output structures. Moreover, they support a model of Parkinsonian reflex blink hyperexcitability in which the SNr–SC target projection is critical.