Multidimensional cerebellar computations for flexible kinematic control of movements

Both the environment and our body keep changing dynamically. Hence, ensuring movement precision requires adaptation to multiple demands occurring simultaneously. Here we show that the cerebellum performs the necessary multi-dimensional computations for the flexible control of different movement parameters depending on the prevailing context. This conclusion is based on the identification of a manifold-like activity in both mossy fibers (MF, network input) and Purkinje cells (PC, output), recorded from monkeys performing a saccade task. Unlike MFs, the properties of PC manifolds developed selective representations of individual movement parameters. Error feedback-driven climbing fiber input modulated the PC manifolds to predict specific, error type-dependent changes in subsequent actions. Furthermore, a feed-forward network model that simulated MF-to-PC transformations revealed that amplification and restructuring of the lesser variability in the MF activity is a pivotal circuit mechanism. Therefore, flexible control of movement by the cerebellum crucially depends on its capacity for multi-dimensional computations.

Optimal information loading into working memory in prefrontal cortex

Working memory involves the short-term maintenance of information and is critical in many tasks. The neural circuit mechanisms underlying this information maintenance are thought to rely on persistent activities resulting from attractor dynamics. However, how information is loaded into working memory for subsequent maintenance remains poorly understood. A pervasive assumption is that information loading requires inputs that are similar to the persistent activities expressed during maintenance. Here, we show through mathematical analysis and numerical simulations that optimal inputs are instead largely orthogonal to persistent activities and naturally generate the rich transient dynamics that are characteristic of prefrontal cortex (PFC) during working memory. By analysing recordings from monkeys performing a memory-guided saccade task, and using a novel, theoretically principled metric, we show that PFC exhibits the hallmarks of optimal information loading. Our theory unifies previous, seemingly conflicting theories of memory maintenance based on attractor or purely sequential dynamics, and reveals a normative principle underlying the widely observed phenomenon of dynamic coding in PFC. These results suggest that optimal information loading may be a key component of attractor dynamics characterising various cognitive functions and cortical areas, including long-term memory and navigation in the hippocampus, and decision making in the PFC.

The role of fixation disengagement and oculomotor preparation in gap saccade task is gap-duration dependent

The influence of internal brain state on behavioral performance is well illustrated by the gap-saccade task, in which saccades might be initiated with short latency (express saccade) or with long latency (regular saccade) even though the external visual condition is identical. Accumulated evidence has demonstrated that the internal brain state is different before the initiation of an express saccade than of a regular saccade. However, the reported origin of the fluctuation of internal brain state is disputed among previous studies, e.g., the fixation disengagement theory versus the oculomotor preparation theory. In the present study, we examined these two theories by analyzing the rate and direction of fixational saccades, i.e., small amplitude saccades during fixation period, because they could be modulated by internal brain state. Since fixation disengagement is not spatially tuned, it might affect the rate but not direction of fixational saccade. In contrast, oculomotor preparation can contain the spatial information for upcoming saccade, thus, it might have a distinct effect on fixational saccade direction. We found that the different spatiotemporal characteristics of fixational saccades among tasks with different gap durations reveals different driven force to change the internal brain state. Under short gap duration (100 ms), fixation disengagement plays a primary role in switching internal brain state. Conversely, under medium (200 ms) and long (400 ms) gap durations, oculomotor preparation plays a primary role. These results suggest that both fixation disengagement and oculomotor preparation can change the internal brain state, but their relative contributions are gap-duration dependent.

Neural mechanisms underlying the temporal control of sequential saccade planning in the frontal eye field

Sequences of saccadic eye movements are instrumental in navigating our visual environment. While neural activity has been shown to ramp up to a threshold before single saccades, the neural underpinnings of multiple saccades is unknown. To understand the neural control of saccade sequences, we recorded from the frontal eye field (FEF) of macaque monkeys while they performed a sequential saccade task. We show that the concurrent planning of two saccade plans brings forth processing bottlenecks, specifically by decreasing the growth rate and increasing the threshold of saccade-related ramping activity. The rate disruption affected both saccade plans, and a computational model, wherein activity related to the two saccade plans mutually and asymmetrically inhibited each other, predicted the behavioral and neural results observed experimentally. Borrowing from models in psychology, our results demonstrate a capacity-sharing mechanism of processing bottlenecks, wherein multiple saccade plans in a sequence compete for the processing capacity by the perturbation of the saccade-related ramping activity. Finally, we show that, in contrast to movement-related neurons, visual activity in FEF neurons is not affected by the presence of multiple saccade targets, indicating that, for perceptually simple tasks, inhibition within movement-related neurons mainly instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.

Correlated variability in primate superior colliculus depends on functional class

Correlated variability (spike count correlations, rSC) in a population of neurons can constrain how information is read out, depending on behavioral task and neuronal tuning. Here we tested whether rSC also depends on neuronal functional class. We recorded from populations of neurons in macaque superior colliculus (SC), a structure that contains well-defined functional classes. We found that during a guided saccade task, different classes of neurons exhibited differing degrees of rSC. "Delay class" neurons displayed the highest rSC, especially during the delay epoch of saccade tasks that relied on working memory. This was only present among Delay class neurons within the same hemisphere. The dependence of rSC on functional class indicates that subpopulations of SC neurons occupy distinct circuit niches with distinct inputs. Such subpopulations should be accounted for differentially when attempting to model or infer population coding principles in the SC, or elsewhere in the primate brain.

Cerebellar complex spikes multiplex complementary behavioral information

Purkinje cell (PC) discharge, the only output of cerebellar cortex, involves 2 types of action potentials, high-frequency simple spikes (SSs) and low-frequency complex spikes (CSs). While there is consensus that SSs convey information needed to optimize movement kinematics, the function of CSs, determined by the PC’s climbing fiber input, remains controversial. While initially thought to be specialized in reporting information on motor error for the subsequent amendment of behavior, CSs seem to contribute to other aspects of motor behavior as well. When faced with the bewildering diversity of findings and views unraveled by highly specific tasks, one may wonder if there is just one true function with all the other attributions wrong? Or is the diversity of findings a reflection of distinct pools of PCs, each processing specific streams of information conveyed by climbing fibers? With these questions in mind, we recorded CSs from the monkey oculomotor vermis deploying a repetitive saccade task that entailed sizable motor errors as well as small amplitude saccades, correcting them. We demonstrate that, in addition to carrying error-related information, CSs carry information on the metrics of both primary and small corrective saccades in a time-specific manner, with changes in CS firing probability coupled with changes in CS duration. Furthermore, we also found CS activity that seemed to predict the upcoming events. Hence PCs receive a multiplexed climbing fiber input that merges complementary streams of information on the behavior, separable by the recipient PC because they are staggered in time.

Memory-Guided Saccades in Psychosis: Effects of Medication and Stimulus Location

The memory-guided saccade task requires the remembrance of a peripheral target location, whilst inhibiting the urge to make a saccade ahead of an auditory cue. The literature has explored the endophenotypic deficits associated with differences in target laterality, but less is known about target amplitude. The data presented came from Crawford et al. (1995), employing a memory-guided saccade task among neuroleptically medicated and non-medicated patients with schizophrenia (n = 31, n = 12), neuroleptically medicated and non-medicated bipolar affective disorder (n = 12, n = 17), and neurotypical controls (n = 30). The current analyses explore the relationships between memory-guided saccades toward targets with different eccentricities (7.5° and 15°), the discernible behaviour exhibited amongst diagnostic groups, and cohorts distinguished based on psychotic symptomatology. Saccade gain control and final eye position were reduced among medicated-schizophrenia patients. These metrics were reduced further among targets with greater amplitudes (15°), indicating greater deficit. The medicated cohort exhibited reduced gain control and final eye positions in both amplitudes compared to the non-medicated cohort, with deficits markedly observed for the furthest targets. No group differences in symptomatology (positive and negative) were reported, however, a greater deficit was observed toward the larger amplitude. This suggests that within the memory-guided saccade paradigm, diagnostic classification is more prominent in characterising disparities in saccade performance than symptomatology.

GazeBase, a large-scale, multi-stimulus, longitudinal eye movement dataset

This manuscript presents GazeBase, a large-scale longitudinal dataset containing 12,334 monocular eye-movement recordings captured from 322 college-aged participants. Participants completed a battery of seven tasks in two contiguous sessions during each round of recording, including a – (1) fixation task, (2) horizontal saccade task, (3) random oblique saccade task, (4) reading task, (5/6) free viewing of cinematic video task, and (7) gaze-driven gaming task. Nine rounds of recording were conducted over a 37 month period, with participants in each subsequent round recruited exclusively from prior rounds. All data was collected using an EyeLink 1000 eye tracker at a 1,000 Hz sampling rate, with a calibration and validation protocol performed before each task to ensure data quality. Due to its large number of participants and longitudinal nature, GazeBase is well suited for exploring research hypotheses in eye movement biometrics, along with other applications applying machine learning to eye movement signal analysis. Classification labels produced by the instrument’s real-time parser are provided for a subset of GazeBase, along with pupil area.