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Jagadisan, U. K.

Publications and source records attributed to Jagadisan, U. K..

4 recordsLinked to original sources

Instantaneous midbrain control of saccade kinematics

The ability to interact with our environment requires the brain to transform spatially-represented sensory signals into temporally-encoded motor commands for appropriate control of the relevant effectors. For visually-guided eye movements, or saccades, the superior colliculus (SC) is assumed to be the final stage of spatial representation, and instantaneous control of the movement is achieved through a rate code representation in the lower brain stem. We questioned this dogma and investigated whether SC activity also employs a dynamic rate code, in addition to the spatial representation. Noting that the kinematics of repeated movements exhibits trial-to-trial variability, we regressed instantaneous SC activity with instantaneous eye velocity and found a robust correlation throughout saccade duration. Peak correlation was tightly linked to time of peak velocity, and SC neurons with higher firing rates exhibited stronger correlations. Moreover, the strong correlative relationship was preserved when eye movement profiles were substantially altered by a blink-induced perturbation. These results indicate that the rate code of individual SC neurons can control instantaneous eye velocity, similar to how primary motor cortex controls hand movements, and argue against a serial process for transforming spatially encoded information into a rate code.

neuroscience

Removal Of Inhibition Uncovers Latent Movement Preparation Dynamics

The motor system prepares for movements well in advance of their execution. In the gaze control system, premotor neurons that produce a burst of activity for the movement are also active leading up to the saccade. The dynamics of preparatory neural activity have been well described by stochastic accumulator models, and variability in the accumulation dynamics has been shown to be correlated with reaction times of the eventual saccade, but it is unclear whether this activity is purely preparatory in nature or has features indicative of a hidden movement command. We explicitly tested whether preparatory neural activity in premotor neurons of the primate superior colliculus has \"motor potential\". We removed inhibition on the saccadic system using reflex blinks, which turn off downstream gating, and found that saccades can be initiated before underlying activity reaches levels seen under normal conditions. Accumulating low-frequency activity was predictive of eye movement dynamics tens of milliseconds in advance of the actual saccade, indicating the presence of a latent movement command. We also show that reaching threshold is not a necessary condition for movement initiation, contrary to the postulates of accumulation-to-threshold models. The results bring into question extant models of saccade generation and support the possibility of a concurrent representation for movement preparation and generation.\n\nSignificance StatementHow the brain plans for upcoming actions before deciding to initiate them is a central question in neuroscience. Popular theories suggest that movement planning and execution occur in serial stages, separated by a decision boundary in neural activity space (e.g., \"threshold\"), which needs to be crossed before the movement is executed. By removing inhibitory gating on the motor system, we show here that the activity required to initiate a saccade can be flexibly modulated. We also show that evolving activity during movement planning is a hidden motor command. The results have important implications for our understanding of how movements are generated, in addition to providing useful information for decoding movement intention based on planning-related activity.\n\nImpact StatementNon-invasive disinhibition of the oculomotor system shows that ongoing preparatory activity in the superior colliculus has movement-generating potential and need not rise to threshold in order to produce a saccade.

neuroscience

Population Temporal Structure Supplements The Rate Code During Sensorimotor Transformations

Sensorimotor transformations are mediated by premotor brain networks where individual neurons represent sensory, cognitive, and movement-related information. Such multiplexing poses a conundrum - how does a decoder know precisely when to initiate a movement if its inputs are active at times when a movement is not desired (e.g., in response to sensory stimulation)? Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate, but critically by a reliable temporal pattern in the population response. Laminar recordings in the superior colliculus (SC), a midbrain region that plays an essential role in orienting eye movements, indicate that the temporal structure across neurons is a factor governing movement initiation. Specifically, using a measure that captures the fidelity of the population code - here called temporal stability - we show that the temporal structure fluctuates during the visual response but becomes increasingly stable during the movement command, even when the mean population activity is similar between the two epochs. Analyses of pseudo-populations in SC and cortical frontal eye fields (FEF) corroborated this model. We also used spatiotemporally patterned microstimulation to causally test the contribution of population temporal stability to movement initiation and found that stable stimulation patterns were more likely to evoke a movement, even when other features of the patterns such as mean pulse rates and population state subspaces were matched. Finally, a spiking neuron model was able to discriminate between stable and unstable input patterns, providing a putative biophysical mechanism for decoding temporal structure. These findings offer an alternative perspective on the relationship between movement preparation and generation by situating the correlates of movement initiation in the temporal features of activity in shared neural substrates. They also suggest a need to look beyond the instantaneous rate code at the single neuron or population level and consider the effects of short-term population history on neuronal communication and behaviour. SummarySensorimotor transformations are mediated by premotor brain networks where individual neurons represent sensory, cognitive, and movement-related information. Such multiplexing poses a conundrum - how does a decoder know precisely when to initiate a movement if its inputs are active at times when a movement is not desired (e.g., in response to sensory stimulation)? Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate, but critically by a reliable temporal pattern in the population response. Laminar recordings in the macaque superior colliculus (SC), a midbrain hub of orienting control, and pseudo-population analyses in SC and cortical frontal eye fields (FEF) corroborated this hypothesis. Importantly, we used spatiotemporally patterned microstimulation to causally verify the importance of temporal structure and demonstrate its role in gating movement initiation. We also offer a spiking neuron model with dendritic integration as a putative mechanism to decode this temporal information. These findings offer new insights into the long-standing debate on movement generation and highlight the importance of short-term population history in neuronal communication and behavior.

neuroscience

Extracting Saccades From Eye Movements Triggered By Reflex Blinks

The trigeminal blink reflex can be evoked by delivering an air puff to the eye. If timed appropriately, e.g., during motor preparation, the small, loopy blink-related eye movement (BREM) associated with eyelid closure disinhibits the saccadic system and reduces the reaction time of planned eye movements. The BREM and intended eye movement overlap temporally, thus a mathematical formulation is required to objectively extract saccade features - onset time and velocity profile - from the combined movement. While it has been assumed that the interactions are nonlinear, we show that blink-triggered movements can be modeled as a linear combination of a typical BREM and a normal saccade, crucially, with an imposed delay between the two components. Saccades reconstructed with this approach are largely similar to control movements in their temporal and spatial profiles. Furthermore, activity profiles of saccade-related bursts in superior colliculus neurons for the recovered saccades closely match those for normal saccades. Thus, blink perturbations, if properly accounted for, offer a non-invasive tool to probe the behavioral and neural signatures of sensory-to-motor transformations.\n\nNew and noteworthyThe trigeminal blink reflex is a brief noninvasive perturbation that disinhibits the saccadic system and provides a behavioral readout of the latent motor preparation process. The saccade, however, is combined with a loopy blink related eye movement. Here, we provide a mathematical formulation to extract the saccade from the combined movement. Thus, blink perturbations, when properly accounted for, offer a non-invasive tool to probe the behavioral and neural signatures of sensory-to-motor transformations.

neuroscience