Development of a neural circuit in the superior colliculus: analysis of the propagation of neuronal excitation from intermediate to superficial layers.

The superior colliculus is important for orientation behaviors, in which visuomotor transformation is performed by the pathway from the superficial layer (SGS) to the intermediate layers (SGI). The opposite pathway (from the SGI to the SGS) also exists, raising the possibility of a feedback circuit, although it could be either negative (inhibitory) or positive (excitatory). In this study, we focused on the development of the feedback circuit. We used optical imaging methods that can measure neuronal population responses directly, as the orientation behaviors are determined by large population activities of superior colliculus neurons. We examined the postnatal development of the propagation pattern of neuronal excitation from the SGI to the SGS using a GABAA receptor antagonist. The optical response propagated within the SGI, but not to the SGS in infant mice that have not opened their eyes. In contrast, in young mice after eye opening, the optical response propagated initially in the SGI and then to the SGS. The GABAA receptor antagonist increased the optical response in the SGS in young mice, as well as that in the SGI in infant mice. Together, these results suggest that axons of SGI neurons terminate to the SGS during development after eye opening.

[Development of a cognitive BMI "neurocommunicator" as a communication aid of patients with severe motor deficits].

A cognitive brain-machine interface (BMI), "neurocommunicator" has been developed by the author's research group in AIST in order to support communication of patients with severer motor deficits. The system can identify candidate messages (pictograms) in real time from electroencephalography (EEG) data, combining three core technologies; 1) a portable/wireless EEG recorder; 2) a high-speed and high-accuracy decoding algorithm; and 3) a hierarchical message generation system. The accuracy of the model at single predictions of the target was generally over 95%, corresponding to about 32 bits per minute for normal subjects. Monitor experiments have been also started for patients at their home, in which further technical improvements are required.

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.

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 monkey's 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.

Dual diffusion model for single-cell recording data from the superior colliculus in a brightness-discrimination task.

Monkeys made saccades to one of two peripheral targets based on the brightness of a central stimulus. Task difficulty was manipulated by varying the ratio of stimulus black-and-white pixels. Correct response probability for two monkeys varied directly with difficulty. Deep layer SC neurons exhibited robust presaccadic activity the magnitude of which was unaffected by task difficulty when the stimulus specified a saccade toward a target within the neuron's response field. Activity after stimuli specifying saccades to targets outside the response field was affected by task difficulty, increasing as the task became more difficult. A quantitative model derived from studies of human decision-making was fit to the behavioral data. The model assumes that information from the stimulus drives two independent diffusion processes. Simulated paths from the model were compared with neuron activity, assuming that firing rate is linearly related to position in the accumulation process. The firing rate data show delayed availability of discriminative information for fast, intermediate, and slow decisions when activity is aligned on the stimulus and very small differences in discriminative information when aligned on the saccade. The model produces exactly these patterns of results. The accumulation process is highly variable, allowing the process both to make errors, as is the case for the behavioral performance, and also to account for the firing rate results. Thus the dual diffusion model provides a quantitative account for both the behavior in a simple decision-making task as well as the patterns of activity in competing populations of neurons.

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 monkey's 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.

Prefrontal neurons coding suppression of specific saccades.

The prefrontal cortex has been implicated in the suppression of unwanted behavior, based upon observations of humans and monkeys with prefrontal lesions. Despite this, there has been little direct neurophysiological evidence for a mechanism that suppresses specific behavior. In this study, we used an oculomotor delayed match/nonmatch-to-sample task in which monkeys had to remember a stimulus location either as a marker of where to look or as a marker of where not to look. We found a group of neurons in both the frontal eye field and the caudal prefrontal cortex that carried signals selective for the forbidden stimulus. The activity of these "don't look" neurons correlated with the monkeys' success or failure on the task. These results demonstrate a frontal signal that is related to the active suppression of one action while the subject performs another.

Neurons in monkey prefrontal cortex whose activity tracks the progress of a three-step self-ordered task.

The self-ordered task is a powerful tool for the analysis of dorsal prefrontal deficits. Each trial consists of a number of steps, and subjects must remember their choices in previous steps. The task becomes more difficult as the number of objects to be remembered increases. We recorded the activity of 156 neurons in the mid-dorsal prefrontal cortex of two rhesus monkeys performing an oculomotor version of the task. Although the task requires working memory, there was no convincing evidence for activity selective for the working memory of the objects that the monkey had to remember. Instead, nearly one-half of neurons (47%, 74/156) showed activity that was modulated according to the step of the task in any one or more task periods. Although the monkey's reward also increased with step, the neurons exhibited little or no step modulation in a reward control task in which reward increased without a concurrent increase in task difficulty. The activity of some neurons was also selective for the location of saccade target that the monkey voluntarily chose. Neurons showed less step modulation in error trials, and there was no increase between the second and third step responses on trials in which the error was on the third step. These results suggest that the mid-dorsal prefrontal cortex contributes to the self-ordered task, not by providing an object working memory signal, but by regulating some general aspect of the performance in the difficult task.