Biology subjects

Corneil, B. D.

Publications and source records attributed to Corneil, B. D..

29 records · Page 2Linked to original sources

bioRxiv2021

High contrast, moving targets in an emerging target paradigm promote fast visuomotor responses during visually guided reaching

Humans have a remarkable capacity to rapidly interact with the surrounding environment, often by transforming visual input into motor output on a moment-to-moment basis. But what visual features promote rapid reaching? High contrast, fast-moving targets elicit strong responses in the superior colliculus (SC), a structure associated with express saccades and implicated in rapid electromyographic (EMG) responses on upper limb muscles. To test the influence of stimulus properties on rapid reaches, we had human subjects perform visually guided reaches to moving targets varied by speed (experiment 1) or speed and contrast (experiment 2), in an emerging target paradigm which has recently been shown to robustly elicit fast visuomotor responses. Our analysis focused on stimulus-locked responses (SLRs) on upper limb muscles. SLRs appear within <100 ms of target presentation, and as the first wave of muscle recruitment, they have been hypothesized to arise from the SC. Across 32 subjects studied in both experiments, 97% expressed SLRs in the emerging target paradigm, whereas only 69% expressed SLRs in an immediate response paradigm towards static targets. Faster moving targets (experiment 1) evoked large magnitude SLRs, while high contrast fast moving targets (experiment 2) evoked short latency, large magnitude SLRs. In some instances, SLR magnitude exceeded the magnitude of movement aligned activity. Both large magnitude and short latency SLRs were correlated with short latency reach reaction times. Our results support the hypothesis that, in scenarios requiring expedited responses, a subcortical pathway originating in the SC elicits the earliest wave of muscle recruitment, expediting reaction times. New & NoteworthyHow does the brain rapidly transform vision into action? Here, by recording upper limb muscle activity, we find that high contrast and fast moving targets are highly effective at evoking rapid visually guided reaches. We surmise that a brainstem circuit originating in the superior colliculus contributes to the most rapid reaching responses. When time is of the essence, cortical areas may serve to prime this circuit, and elaborate subsequent phases of recruitment.

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bioRxiv2020

The influence of temporal predictability on express visuomotor responses

Volitional visuomotor responses in humans are generally thought to manifest 100ms or more after stimulus onset. Under appropriate conditions, however, much faster target-directed responses can be produced at upper limb and neck muscles. These "express" responses have been termed stimulus-locked responses (SLRs) and are proposed to be modulated by visuomotor transformations performed subcortically via the superior colliculus. Unfortunately, for those interested in studying SLRs, these responses have proven difficult to detect consistently across individuals. The recent report of an effective paradigm for generating SLRs in 100% of participants appears to change this. The task required the interception of a moving target that emerged from behind a barrier at a time consistent with the target velocity. Here we aimed to reproduce the efficacy of this paradigm for eliciting SLRs and to test the hypothesis that its effectiveness derives from the predictability of target onset time as opposed to target motion per se. In one experiment, we recorded surface EMG from shoulder muscles as participants made reaches to intercept temporally predictable or unpredictable targets. Consistent with our hypothesis, predictably timed targets produced more frequent and stronger SLRs than unpredictably timed targets. In a second experiment, we compared different temporally predictable stimuli and observed that transiently presented targets produced larger and earlier SLRs than sustained moving targets. Our results suggest that target motion is not critical for facilitating the expression of an SLR and that timing predictability does not rely on extrapolation of a physically plausible motion trajectory. These findings provide support for a mechanism whereby an internal timer, probably located in cerebral cortex, primes the processing of both visual input and motor output within the superior colliculus to produce SLRs.

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bioRxiv2020

An emerging target paradigm evokes fast visuomotor responses on human upper limb muscles

To reach towards a seen object, visual information has to be transformed into motor commands. Visual information such as the objects colour, shape, and size is processed and integrated within numerous brain areas, then ultimately relayed to the motor periphery. In some instances we must react as fast as possible. These fast visuomotor transformations, and their underlying neurological substrates, are poorly understood in humans as they have lacked a reliable biomarker. Stimulus-locked responses (SLRs) are short latency (<100 ms) bursts of electromyographic (EMG) activity representing the first wave of muscle recruitment influenced by visual stimulus presentation. SLRs provide a quantifiable output of rapid visuomotor transformations, but SLRs have not been consistently observed in all subjects in past studies. Here we describe a new, behavioural paradigm featuring the sudden emergence of a moving target below an obstacle that consistently evokes robust SLRs. Human participants generated visually-guided reaches toward or away from the emerging target using a robotic manipulandum while surface electrodes recorded EMG activity from the pectoralis major muscle. In comparison to previous studies that investigated SLRs using static stimuli, the SLRs evoked with this emerging target paradigm were larger, evolved earlier, and were present in all participants. Reach reaction times (RTs) were also expedited in the emerging target paradigm. This paradigm affords numerous opportunities for modification that could permit systematic study of the impact of various sensory, cognitive, and motor manipulations on fast visuomotor responses. Overall, our results demonstrate that an emerging target paradigm is capable of consistently and robustly evoking activity within a fast visuomotor system. SUMMARYWe present a new behavioual paradigm that elicits robust fast visuomotor responses on human upper limb muscles during visually guided reaches.

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bioRxiv2019

From competing motor plans to a single action within a single trial on the human motor periphery

Contemporary motor control theories propose competition between multiple motor plans before the winning command is executed. While most competitions are completed prior to movement onset, movements are often initiated before the competition has been resolved. An example of this is saccadic averaging, wherein the eyes land at an intermediate location between two visual targets. Behavioral and neurophysiological signatures of competing motor commands have also been reported for reaching movements, but debate remains about whether such signatures attest to an unresolved competition, arise from averaging across many trials, or reflect a strategy to optimize behavior given task constraints. Here, we recorded electromyographic activity from an upper limb muscle (m. pectoralis) while twelve (8 female) participants performed an immediate response reach task, freely choosing between one of two identical and suddenly presented visual targets. On each trial, muscle recruitment showed two distinct phases of directionally-tuned activity. In the first wave, time-locked ~100 ms of target presentation, muscle activity was clearly influenced by the non-chosen target, reflecting a competition between reach commands that was biased in favor of the ultimately chosen target. This resulted in an initial movement intermediate between the two targets. In contrast, the second wave, time-locked to voluntary reach onset, was not biased toward the non-chosen target, showing that the competition between targets was resolved. Instead, this wave of activity compensated for the averaging induced by the first wave. Thus, single-trial analysis reveals an evolution in how the non-chosen target differentially influences the first and second wave of muscle activity. SIGNIFICANCE STATEMENTContemporary theories of motor control suggest that multiple motor plans compete for selection before the winning command is executed. Evidence for this is found in intermediate reach movements towards two potential target locations, but recent findings have challenged this notion by arguing that intermediate reaching movements reflect an optimal response strategy. By examining upper limb muscle recruitment during a free-choice reach task, we show early recruitment of a sub-optimal averaged motor command to the two targets that subsequently transitions to a single motor command that compensates for the initially averaged motor command. Recording limb muscle activity permits single-trial resolution of the dynamic influence of the non-chosen target through time.

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bioRxiv2019

Stimulus-Locked Responses on Human Upper Limb Muscles and Corrective Reaches are Preferentially Evoked by Low Spatial Frequencies

In situations requiring immediate action, humans can generate visually-guided responses at remarkably short latencies. Here, to better understand the visual attributes that best evoke such rapid responses, we recorded upper limb muscle activity while participants performed visually-guided reaches towards Gabor patches composed of differing spatial frequencies. We studied reaches initiated from a stable posture (experiment 1, a static condition), or during on-line reach corrections to an abruptly displaced target (experiment 2, a dynamic condition). In both experiments, we detail the latency and prevalence of stimulus-locked responses (SLRs), which are brief bursts of EMG activity that are time-locked to target presentation rather than movement onset. SLRs represent the first wave of EMG recruitment influenced by target presentation, and enable quantification of rapid visuomotor transformations. In both experiments, reach targets composed of low spatial frequencies elicited the shortest latency and most prevalent SLRs, with SLR latency increasing and SLR prevalence decreasing for reach targets composed of progressively higher spatial frequencies. SLRs could be evoked in either the static or dynamic condition, and when present in experiment 2, were associated with shorter latency and larger magnitude corrections. Furthermore, SLRs evolved at shorter latencies (~20 ms) when the arm was already in motion. These results demonstrate that stimuli composed of low spatial frequencies preferentially evoke the most rapid visuomotor responses which, in the context of rapidly correcting an on-going reaching movement, are associated with earlier and larger on-line reach corrections.\n\nSignificance StatementHumans have a remarkable capacity to respond quickly to changes in our visual environment. Although our visual world is composed of a range of spatial frequencies, surprisingly little is known about which frequencies preferentially evoke rapid reaching responses. Here, we systematically varied the spatial frequency of peripheral reach targets while measuring EMG activity on an upper limb muscle. We found that visual stimuli composed of low-spatial frequencies elicit the most rapid and robust EMG responses and corrective reaches. Thus, when time is of the essence, low spatial frequencies preferentially drive fast visuomotor responses.

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bioRxiv2019

Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

Saccades require a spatiotemporal transformation of activity between the intermediate layers of the superior colliculus (iSC) and downstream brainstem burst generator. The dynamic linear ensemble-coding model (Goossens and Van Opstal, 2006) proposes that each iSC spike contributes a fixed mini-vector to saccade displacement. Although biologically-plausible, this model assumes cortical areas like the frontal eye fields (FEF) simply provide the saccadic goal to be executed by the iSC and brainstem burst generator. However, the FEF and iSC operate in unison during saccades, and a pathway from the FEF to the brainstem burst generator that bypasses the iSC exists. Here, we investigate the impact of large yet reversible inactivation of the FEF on iSC activity in the context of the model across four saccade tasks. We exploit the overlap of saccade vectors generated when the FEF is inactivated or not, comparing the number of iSC spikes for metrically-matched saccades. We found that the iSC emits fewer spikes for metrically-matched saccades during FEF inactivation. The decrease in spike count is task-dependent, with a greater decrease accompanying more cognitively-demanding saccades. Our results show that FEF integrity influences the readout of iSC activity in a task-dependent manner. We propose that the dynamic linear ensemble-coding model be modified so that FEF inactivation increases the gain of a readout parameter, effectively increasing the influence of a single iSC spike. We speculate that this modification could be instantiated by a direct pathway from the FEF to the omnipause region that modulates the excitability of the brainstem burst generator.\n\nSignificance statementOne of the enduring puzzles in the oculomotor system is how it achieves the spatiotemporal transformation, converting spatial activity within the intermediate layers of the superior colliculus (iSC) into a rate code within the brainstem burst generator. The spatiotemporal transformation has traditionally been viewed as the purview of the oculomotor brainstem. Here, within the context of testing a biologically-plausible model of the spatiotemporal transformation, we show that reversible inactivation of the frontal eye fields (FEF) decreases the number of spikes issued by the iSC for metrically-matched saccades, with greater decreases accompanying more cognitively-demanding tasks. These results show that signals from the FEF influence the spatiotemporal transformation.

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bioRxiv2019

Impairment but not abolishment of express saccades after unilateral- or bilateral cryogenic FEF inactivation

Express saccades (ESs) are a manifestation of a visual grasp reflex triggered when visual information arrives in the intermediate layers of the superior colliculus (SCi), which in turn orchestrates the lower level brainstem saccade generator to evoke a saccade with a very short latency ([~]100ms). A prominent theory regarding express saccades generation is that they are facilitated by preparatory signals, presumably from cortical areas, which prime the SCi prior to the arrival of visual information. Here, we test this theory by reversibly inactivating a key cortical input to the SCi, the frontal eye fields (FEF), while monkeys perform an oculomotor task that promotes ES generation. Across three tasks with a different combination of potential target locations and uni- or bilateral FEF inactivation, we found a spared ability for monkeys to generate ESs, despite decreases in ES frequency during FEF inactivation. This result is consistent with the FEF having a facilitatory but not critical role in ES generation, likely because other cortical areas compensate for the loss of preparatory input to the SCi. However, we did find decreases in the accuracy and peak velocity of ESs generated during FEF inactivation, which argues for an influence of the FEF on the saccadic burst generator even during ESs. Overall, our results shed further light on the role of the FEF in the shortest-latency visually-guided eye movements.\n\nNew & NoteworthyExpress saccades (ESs) are the shortest-latency visually-guided saccade. The frontal eye fields (FEF) is thought to promote ES by establishing the necessary preconditions in the superior colliculus. Here, by reversibly inactivate the FEF either unilaterally or bilaterally, we support this view by showing that the FEF plays an assistive but not critical role in ES generation. We also found that FEF inactivation lowered ES peak velocity, emphasizing a contribution of the FEF to ES kinematics.

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bioRxiv2018

A rapid visuomotor response on the human upper limb is selectively influenced by implicit, but not explicit, motor learning

How do humans learn to adapt their motor actions to achieve task success? Recent behavioral and patient studies have challenged the classic notion that motor learning arises solely from the errors produced during a task, suggesting instead that explicit cognitive strategies can act in concert with the implicit, error\"based, motor learning component. Here, we show that the earliest wave of directionally-tuned neuromuscular activity that occurs within ~100 ms of peripheral visual stimulus onset is selectively influenced by the implicit component of motor learning. In contrast, the voluntary neuromuscular activity associated with reach initiation, which evolves ~100 to 200 ms later is influenced by both the implicit and explicit components of motor learning. The selective influence of the implicit, but not explicit, component of motor learning on the earliest cascade of neuromuscular activity supports the notion that these components of motor learning can differentially influence descending motor pathways.

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bioRxiv2017

Frontal eye field inactivation reduces saccade preparation in the superior colliculus, but does not alter how preparatory activity relates to saccade latency

A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of preparatory activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of iSC preparatory activity precede shorter SRTs. The frontal eye fields (FEF) are one likely source of such iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEFs role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys we examined iSC preparatory activity during unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced fixation-related activity in the rostral iSC. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. These analyses revealed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades, suggesting that the integration of preparatory and visual signals in the SC just before saccade initiation is largely independent of the FEF for saccades generated in this task.\n\nSignificance statementHow does the brain decide when to move? Here, we investigate the role of two oculomotor structures, the superior colliculus (SC) and frontal eye fields (FEF), in dictating visually-guided saccadic reaction times (SRTs). In both structures, higher levels of preparatory activity precede shorter SRTs. Here, we show that FEF inactivation increases SRTs and decreases SC preparatory activity. Surprisingly, a population-level analysis of SC preparatory activity showed a negligible impact of FEF inactivation, providing one examines SRT-matched saccades. Thus, while the FEF is one source of preparatory input to the SC, it is not a critical source, and it is not involved in the integration of preparatory activity and visual signals that precedes saccade initiation in simple visually-guided saccade tasks.

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bioRxiv2017

Done in 100 ms: Path-dependent visuomotor transformation in the human upper limb

A core assumption underlying mental chronometry is that more complex tasks increase cortical processing, prolonging reaction times. Here we show that increases in task complexity alter the magnitude, rather than the latency, of the output for a circuit that rapidly transforms visual information into motor actions. We quantified visual stimulus-locked responses (SLRs), which are changes in upper limb muscle recruitment that evolve at a fixed latency [~]100 ms after novel visual stimulus onset. First, we studied the underlying reference frame of the SLR, by dissociating initial eye and hand position. Despite its quick latency, we found that the SLR was expressed in a hand-centric reference frame, suggesting that the circuit mediating the SLR integrated retinotopic visual information with body configuration. Next, we studied the influence of planned movement trajectory, requiring participants to prepare and generate curved or straight reaches in the presence of obstacles to attain the same visual stimulus. We found that SLR magnitude reflected the initial planned movement trajectory, regardless of the ensuing movement curvature. Based on these results, we suggest that the circuit mediating the SLR lies in parallel to other well-studied corticospinal pathways. Although the fixed latency of the SLR precludes extensive cortical processing, inputs conveying information relating to task complexity, such as body configuration and planned movement trajectory, can pre-set nodes within the circuit underlying to the SLR to modulate its magnitude.\n\nSIGNIFICANCE STATEMENTA core assumption underlying mental chronometry is that more complex tasks increase cortical processing, prolonging reaction times. Here, we showed that increases in task complexity altered the magnitude, rather than the latency, of a circuit that rapidly transforms visual information into motor actions. We focus on stimulus-locked responses (SLRs), which are changes in upper limb muscle recruitment that evolve at a fixed latency [~]100 ms after novel visual stimulus onset. We showed that despite is quick latency, the circuitry mediating the SLR transformed a retinotopic visual signal into a hand-centric motor command suitable to contribute to the initial movement trajectory. We suggest that this circuit lies in parallel to other well-studied corticospinal pathways.

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bioRxiv2017

Frontal Eye Field inactivation diminishes Superior Colliculus activity, but delayed saccadic accumulation governs reaction time increases

Stochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEF) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation, by relating variations in saccade reaction time (SRT) to variations in parameters such as baseline, rate of accumulation of activity, or threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in non-human primates, we causally test which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation.\n\nSignificance StatementThe superior colliculus (SC) and frontal eye fields (FEF) are two of the best-studied areas in the primate brain. Surprisingly, little is known about what happens in the SC when the FEF is temporarily inactivated. Here, we show that temporary FEF inactivation decreases all aspects of functionally-related activity in the SC. This combination of techniques also allowed us to relate changes in SC activity to concomitant increases in saccadic reaction time (SRT). Although stochastic accumulator models relate SRT increases to reduced rates of accumulation or increases in threshold, such changes were not observed in the SC. Instead, FEF inactivation delayed the onset of saccade-related accumulation, emphasizing the importance of this parameter in biologically-plausible models of saccade initiation.

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