Neeraj J. Gandhi

Our study uses microsimulation at multiple sites in the frontal eye fields to investigate the principles by which its outputs are integrated to form a unified saccadic eye movement. We provide evidence for a new model governing this integration and evaluate that model for microstimulation in both the frontal eye fields and the superior colliculus.

Moving targets pose a fundamental challenge for sensorimotor control: by the time a target's position is transformed into neural signals, the target has already moved. Primates compensate for this delay and accurately intercept objects by accounting for target velocity. However, the neural mechanisms by which sensorimotor structures represent target velocity remain poorly understood. Here we recorded spikes and local field potentials from the superior colliculus (SC) of male macaques viewing or directing saccades to stationary and moving targets and used time-resolved dimensionality reduction and classification to characterize SC population dynamics. Target velocity emerged rapidly within the visual response and was robustly decodable despite weak and inconsistent single-neuron motion sensitivity. In low-dimensional state space, activity formed a V-shaped manifold in which speed was organized continuously along direction-specific arms. This geometry generalized across animals and signal modalities, could not be reproduced by displacement-based simulations, and remained largely dissociable from the axis encoding target location. Velocity information was strongest near the border between superficial and intermediate layers, identifying a laminar locus where visual motion signals may be transformed into commands for interception. These findings reveal separate, partially overlapping geometries for representation of target speed and position in the SC and overturn the longstanding view that it encodes only target location and movement goals.

Sensorimotor transformation, the process of converting sensory input signals into a movement command, is essential for mediating goal-directed movements. Neural correlates of sensorimotor transformation were assessed in the delay period activity of superior colliculus (SC) neurons recorded simultaneously in three male monkeys generating saccades to visual targets. We applied dimensionality reduction on the SC population response and used a proximity index to quantify the relative, probabilistic closeness of the evolving delay period activity to the visual- and motor-dominant subspaces associated with the sensation and action states. Here, we show that sensorimotor transformation is achieved through a drift in population activity from a visual-like to a motor-like representation during the delay period, with transient visual resets following microsaccades. Also, the proximity index was correlated to reaction time throughout the delay period, suggesting a similar movement preparation mechanism is conserved across the skeletomotor and oculomotor systems.

The frontal eye field (FEF), a region of frontal cortex, has long been associated with the cortical control of eye movements. Classically, saccades can be reliably evoked by delivering low-intensity electrical microstimulation to the FEF. Although this makes clear the importance of FEF in the descending control of eye movements, the way in which population activity in the FEF is integrated by downstream regions to generate a motor command remains a mystery. To probe these mechanisms, we used a 16-channel microelectrode array to deliver microstimulation to the FEF of two awake, behaving monkeys. First, we found that larger current intensities were required to evoke changes in saccade direction relative to saccade amplitude when single-site saccades were evoked by stimulating a single contact on the array. Second, when stimulating two contacts simultaneously to investigate how population activity in the FEF is read out, a new polar average model more accurately predicted the amplitude and direction of dual-site saccades than traditional vector sum and vector average models. Using preexisting data from the superior colliculus (SC), we found that although the polar average model was more accurate at predicting saccade amplitude in the SC, it was no more accurate than traditional models at predicting saccade direction. Finally, when stimulating two contacts in FEF simultaneously with unequal current intensities, model accuracy depended on the amplitude of the saccades evoked by stimulating each individual site alone, suggesting that the brain may flexibly combine amplitude and direction information from the FEF to generate saccadic plans.

Neural signals encode information through oscillatory and transient components. The transient component captures rapid, non-rhythmic changes in response to internal or external events, while the oscillatory component reflects rhythmic patterns critical for processing sensation, action, and cognition. Current spectral and time-domain methods often struggle to distinguish the two components, particularly under sharp transitions, leading to interference and spectral leakage. This study introduces a novel adaptive smoothing algorithm that isolates oscillatory and transient components by dynamically up-sampling signal regions with abrupt changes. The approach leverages Euclidean distance-based thresholds to refine sampling and applies customized smoothing techniques, preserving transient details while minimizing interference. Tested on both synthetic and recorded local field potential data, the algorithm outperformed conventional methods in handling steep signal transitions, as demonstrated by lower mean-square error and improved spectral separation. Our findings highlight the algorithm’s potential to enhance neural signal analysis by more accurately separating components, paving the way for more precise characterization of neural dynamics in research and clinical applications.

Sensorimotor transformation is the process of first sensing an object in the environment and then producing a movement in response to that stimulus. For visually guided saccades, neurons in the superior colliculus (SC) emit a burst of spikes to register the appearance of stimulus, and many of the same neurons discharge another burst to initiate the eye movement. We investigated whether the neural signatures of sensation and action in SC depend on context. Spiking activity along the dorsoventral axis was recorded with a laminar probe as Rhesus monkeys generated saccades to the same stimulus location in tasks that require either executive control to delay saccade onset until permission is granted or the production of an immediate response to a target whose onset is predictable. Using dimensionality reduction and discriminability methods, we show that the subspaces occupied during the visual and motor epochs were both distinct within each task and differentiable across tasks. Single-unit analyses, in contrast, show that the movement-related activity of SC neurons was not different between tasks. These results demonstrate that statistical features in neural activity of simultaneously recorded ensembles provide more insight than single neurons. They also indicate that cognitive processes associated with task requirements are multiplexed in SC population activity during both sensation and action and that downstream structures could use this activity to extract context. Additionally, the entire manifolds associated with sensory and motor responses, respectively, may be larger than the subspaces explored within a certain set of experiments.

Sensorimotor transformation is the sequential process of registering a sensory signal in the environment and then responding with the relevant movement at an appropriate time. For visually guided eye movements, neural signatures in the form of spiking activity of neurons have been extensively studied along the dorsoventral axis of the superior colliculus (SC). In contrast, the local field potential (LFP), which represents the putative input to a region, remains largely unexplored in the SC. We therefore compared amplitude levels and onset times of both spike bursts and LFP modulations recorded simultaneously with a laminar probe along the dorsoventral axis of SC in 3 male monkeys performing the visually guided delayed saccade task. Both signals displayed a gradual transition from sensory activity in the superficial layers to a predominantly motor response in the deeper layers, although the transition from principally sensory to mostly motor response occurred ∼500 μm deeper for the LFP. For the sensory response, LFP modulation preceded spike burst onset by 25 ms in the deeper layers. The results reveal a fast and efficient input-output transformation between LFP modulation and spike burst in the visually responsive layers activity during sensation but not during action. The spiking pattern observed during the movement phase is likely dominated by intracollicular processing that is not captured in the LFP.SIGNIFICANCE STATEMENTWhat is the sequence of events between local field potential (LFP) modulation and spiking activity during sensorimotor transformation? A trial-by-trial analysis reveals that the LFP activity leads the spike burst in the superficial and intermediate layers of the superior colliculus during visual processing, while both trial-by-trial and the average analyses show that the spike burst leads the LFP modulation during movement generation. These results suggest an almost instantaneous LFP input, spike burst output transformation in the visually responsive layers of the superior colliculus when registering the stimulus. In contrast, substantial intracollicular processing likely results in a saccade-related spike burst that leads LFP modulation.