scholarly journals Removal of inhibition uncovers latent movement potential during preparation

2017 ◽  
Author(s):  
Uday K. Jagadisan ◽  
Neeraj J. Gandhi
Keyword(s):  
Superior Colliculus ◽  
Neural Activity ◽  
Motor System ◽  
Reaction Times ◽  
Motor Command ◽  
Oculomotor System ◽  
Movement Planning ◽  
Necessary Condition ◽  
Movement Initiation ◽  
Premotor Neurons

AbstractThe 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.Significance 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.Impact 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.

scholarly journals Removal of inhibition uncovers latent movement potential during preparation

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Uday K Jagadisan ◽  
Neeraj J Gandhi
Keyword(s):  
Neural Activity ◽  
Low Frequency ◽  
Threshold Level ◽  
Blink Reflex ◽  
Necessary Condition ◽  
Gaze Control ◽  
Movement Initiation ◽  
The Gaze ◽  
Movement Dynamics ◽  
Premotor Neurons

The motor system prepares for movements well in advance of their execution. In the gaze control system, the dynamics of preparatory neural activity have been well described by stochastic accumulation-to-threshold models. However, it is unclear whether this activity 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 downstream inhibition on the saccadic system using the trigeminal blink reflex, triggering saccades at earlier-than-normal latencies. 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 a fixed threshold level is not a necessary condition for movement initiation. The results bring into question extant models of saccade generation and support the possibility of a concurrent representation for movement preparation and generation.

scholarly journals Motor planning modulates neural activity patterns in early human auditory cortex

2019 ◽  
Author(s):  
Daniel J. Gale ◽  
Corson N. Areshenkoff ◽  
Claire Honda ◽  
Ingrid S. Johnsrude ◽  
J. Randall Flanagan ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Neural Activity ◽  
Motor System ◽  
Activity Patterns ◽  
Motor Planning ◽  
Sensory Information ◽  
Action Planning ◽  
Movement Planning ◽  
Specific Information ◽  
Related Information

AbstractIt is well established that movement planning recruits motor-related cortical brain areas in preparation for the forthcoming action. Given that an integral component to the control of action is the processing of sensory information throughout movement, we predicted that movement planning might also modulate early sensory cortical areas, readying them for sensory processing during the unfolding action. To test this hypothesis, we performed two human functional MRI studies involving separate delayed movement tasks and focused on pre-movement neural activity in early auditory cortex, given its direct connections to the motor system and evidence that it is modulated by motor cortex during movement in rodents. We show that effector-specific information (i.e., movements of the left vs. right hand in Experiment 1, and movements of the hand vs. eye in Experiment 2) can be decoded, well before movement, from neural activity in early auditory cortex. We find that this motor-related information is represented in a separate subregion of auditory cortex than sensory-related information and is present even when movements are cued visually instead of auditorily. These findings suggest that action planning, in addition to preparing the motor system for movement, involves selectively modulating primary sensory areas based on the intended action.

Movement Planning Determines Sensory Suppression: An Event-related Potential Study

2021 ◽  
pp. 1-13
Author(s):  
Bradley N. Jack ◽  
Miranda R. Chilver ◽  
Richard M. Vickery ◽  
Ingvars Birznieks ◽  
Klimentina Krstanoska-Blazeska ◽  
...  
Keyword(s):  
Sensory Input ◽  
Event Related Potentials ◽  
Motor Command ◽  
Event Related Potential ◽  
Forward Model ◽  
Movement Planning ◽  
Necessary Condition ◽  
Sensory Suppression ◽  
Internal Forward Model ◽  
Related Potentials

Abstract Sensory suppression refers to the phenomenon that sensory input generated by our own actions, such as moving a finger to press a button to hear a tone, elicits smaller neural responses than sensory input generated by external agents. This observation is usually explained via the internal forward model in which an efference copy of the motor command is used to compute a corollary discharge, which acts to suppress sensory input. However, because moving a finger to press a button is accompanied by neural processes involved in preparing and performing the action, it is unclear whether sensory suppression is the result of movement planning, movement execution, or both. To investigate this, in two experiments, we compared event-related potentials to self-generated tones that were produced by voluntary, semivoluntary, or involuntary button-presses, with externally generated tones that were produced by a computer. In Experiment 1, the semivoluntary and involuntary button-presses were initiated by the participant or experimenter, respectively, by electrically stimulating the median nerve in the participant's forearm, and in Experiment 2, by applying manual force to the participant's finger. We found that tones produced by voluntary button-presses elicited a smaller N1 component of the event-related potential than externally generated tones. This is known as N1-suppression. However, tones produced by semivoluntary and involuntary button-presses did not yield significant N1-suppression. We also found that the magnitude of N1-suppression linearly decreased across the voluntary, semivoluntary, and involuntary conditions. These results suggest that movement planning is a necessary condition for producing sensory suppression. We conclude that the most parsimonious account of sensory suppression is the internal forward model.

Influence of Task Predictability on the Activity of Neurons in the Rostral Superior Colliculus During Double-Step Saccades

2009 ◽  
Vol 101 (6) ◽  
pp. 3199-3211 ◽  
Author(s):  
Vicente Reyes-Puerta ◽  
Roland Philipp ◽  
Werner Lindner ◽  
Lars Lünenburger ◽  
Klaus-Peter Hoffmann
Keyword(s):  
Superior Colliculus ◽  
Neuronal Activity ◽  
Neural Activity ◽  
Learning Effect ◽  
Reaction Times ◽  
Neuronal Responses ◽  
Top Down ◽  
Double Step ◽  
Target Probability ◽  
Preparatory Activity

Target probability has been shown to modulate motor preparatory activity of neurons in the caudal superior colliculus (SC) of the primate. Here we tested whether top-down processes, such as task predictability, influence the activity of neurons also at the rostral pole of the SC (rSC), classically related to fixation. To investigate this, double-step saccade tasks were embedded in two different paradigms, one containing unpredictable and another containing predictable tasks. During predictable tasks the animals could develop some expectation about the forthcoming second target jump, i.e., anticipate when and where to make the second saccade. Neuronal responses were recorded during both paradigms and compared, revealing the influence of task predictability on the activity of rSC neurons during specific periods of fixation. In particular, neuronal activity stayed significantly lower during the fixation period between two successive saccades in predictable than in unpredictable tasks. In addition there was a learning effect within a session during predictable conditions, i.e., the intersaccadic activity was higher in the early than in the late trials. Further, reaction times for the second saccade were shorter in predictable than in unpredictable tasks. However, we demonstrated that this difference in reaction times cannot be solely accounted for by the reported difference in neural activity, which was mainly influenced by the predictability of the tasks. With these results we show that top-down processes such as predictability are imposed on the activity of neurons in the rostral pole of the primate SC.

Neural Organization From the Superior Colliculus to Motoneurons in the Horizontal Oculomotor System of the Cat

1999 ◽  
Vol 81 (6) ◽  
pp. 2597-2611 ◽  
Author(s):  
Y. Izawa ◽  
Y. Sugiuchi ◽  
Y. Shinoda
Keyword(s):  
Superior Colliculus ◽  
Reticular Formation ◽  
Wheat Germ ◽  
Abducens Nerve ◽  
Vestibular Nuclei ◽  
Oculomotor System ◽  
Abducens Nucleus ◽  
Axon Terminals ◽  
Neural Organization ◽  
Premotor Neurons

Neural organization from the superior colliculus to motoneurons in the horizontal oculomotor system of the cat. The neural organization of the superior colliculus (SC) projection to horizontal ocular motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling. Intracellular responses to SC stimulation were analyzed in lateral rectus (LR) and medial rectus (MR) motoneurons and internuclear neurons in the abducens nucleus (AINs). LR motoneurons and AINs received excitation from the contralateral SC and inhibition from the ipsilateral SC. The shortest excitation (0.9–1.9 ms) and inhibition (1.4–2.4 ms) were mainly disynaptic from the SC and were followed by tri- and polysynaptic responses evoked with increasing stimuli or intensity. All MR motoneurons received excitation from the ipsilateral SC, whereas none of them received any short-latency inhibition from the contralateral SC, but some received excitation. The latency of the ipsilateral excitation in MR motoneurons (1.7–2.8 ms) suggested that this excitation was trisynaptic via contralateral AINs, because conditioning SC stimulation spatially facilitated trisynaptic excitation from the ipsilateral vestibular nerve. To locate interneurons mediating the disynaptic SC inputs to LR motoneurons, last-order premotor neurons were labeled transneuronally after injecting wheat germ agglutinin–conjugated horseradish peroxidase into the abducens nerve, and tectoreticular axon terminals were labeled after injecting dextran-biotin into the ipsilateral or contralateral SC in the same preparations. Transneuronally labeled neurons were mainly distributed ipsilaterally in the paramedian pontine reticular formation (PPRF) rostral to retrogradely labeled LR motoneurons and the vestibular nuclei, and contralaterally in the paramedian pontomedullary reticular formation (PPMRF) caudomedial to the abducens nucleus and the vestibular nuclei. Among the last-order premotor neuron areas, orthogradely labeled tectoreticular axon terminals were observed only in the PPRF and the PPMRF contralateral to the injected SC and seemed to make direct contacts with many of the labeled last-order premotor neurons in the PPRF and the PPMRF. These morphological results confirmed that the main excitatory and inhibitory connections from the SC to LR motoneurons are disynaptic and that the PPRF neurons that receive tectoreticular axon terminals from the contralateral SC terminate on ipsilateral LR motoneurons, whereas the PPMRF neurons that receive tectoreticular axon terminals from the contralateral SC terminate on contralateral LR motoneurons.

scholarly journals Giving Subjects the Eye and Showing Them the Finger: Socio-Biological Cues and Saccade Generation in the Anti-Saccade Task

Perception ◽  
10.1068/p7085 ◽  
2012 ◽  
Vol 41 (2) ◽  
pp. 131-147 ◽  
Author(s):  
Nicola J Gregory ◽  
Timothy L Hodgson
Keyword(s):  
Opposite Direction ◽  
Reaction Times ◽  
Oculomotor System ◽  
Short Soas ◽  
Stimulus Onset ◽  
Saccade Direction ◽  
Saccade Task ◽  
Saccadic Reaction Times ◽  
Saccadic Responses ◽  
Gaze Cues

Pointing with the eyes or the finger occurs frequently in social interaction to indicate direction of attention and one's intentions. Research with a voluntary saccade task (where saccade direction is instructed by the colour of a fixation point) suggested that gaze cues automatically activate the oculomotor system, but non-biological cues, like arrows, do not. However, other work has failed to support the claim that gaze cues are special. In the current research we introduced biological and non-biological cues into the anti-saccade task, using a range of stimulus onset asynchronies (SOAs). The anti-saccade task recruits both top–down and bottom–up attentional mechanisms, as occurs in naturalistic saccadic behaviour. In experiment 1 gaze, but not arrows, facilitated saccadic reaction times (SRTs) in the opposite direction to the cues over all SOAs, whereas in experiment 2 directional word cues had no effect on saccades. In experiment 3 finger pointing cues caused reduced SRTs in the opposite direction to the cues at short SOAs. These findings suggest that biological cues automatically recruit the oculomotor system whereas non-biological cues do not. Furthermore, the anti-saccade task set appears to facilitate saccadic responses in the opposite direction to the cues.

Effects of Local Nicotinic Activation of the Superior Colliculus on Saccades in Monkeys

2005 ◽  
Vol 93 (1) ◽  
pp. 519-534 ◽  
Author(s):  
Masayuki Watanabe ◽  
Yasushi Kobayashi ◽  
Yuka Inoue ◽  
Tadashi Isa
Keyword(s):  
Superior Colliculus ◽  
Reaction Times ◽  
Low Frequency ◽  
Visually Guided ◽  
Population Activity ◽  
Affected Area ◽  
Movement Field ◽  
Neural Interactions ◽  
Restricted Region

To examine the role of competitive and cooperative neural interactions within the intermediate layer of superior colliculus (SC), we elevated the basal SC neuronal activity by locally injecting a cholinergic agonist nicotine and analyzed its effects on saccade performance. After microinjection, spontaneous saccades were directed toward the movement field of neurons at the injection site (affected area). For visually guided saccades, reaction times were decreased when targets were presented close to the affected area. However, when visual targets were presented remote from the affected area, reaction times were not increased regardless of the rostrocaudal level of the injection sites. The endpoints of visually guided saccades were biased toward the affected area when targets were presented close to the affected area. After this endpoint effect diminished, the trajectories of visually guided saccades remained modestly curved toward the affected area. Compared with the effects on endpoints, the effects on reaction times were more localized to the targets close to the affected area. These results are consistent with a model that saccades are triggered by the activities of neurons within a restricted region, and the endpoints and trajectories of the saccades are determined by the widespread population activity in the SC. However, because increased reaction times were not observed for saccades toward targets remote from the affected area, inhibitory interactions in the SC may not be strong enough to shape the spatial distribution of the low-frequency preparatory activities in the SC.

scholarly journals Passive sensorimotor stimulation triggers long lasting alpha-band fluctuations in visual perception

2018 ◽  
Vol 119 (2) ◽  
pp. 380-388 ◽  
Author(s):  
Alice Tomassini ◽  
Alessandro D’Ausilio
Keyword(s):  
Visual Perception ◽  
Median Nerve ◽  
Movement Planning ◽  
Sensorimotor System ◽  
Alpha Power ◽  
Alpha Band ◽  
Movement Initiation ◽  
Visual Contrast ◽  
Sensorimotor Processes ◽  
Stimulation Of

Movement planning and execution rely on the anticipation and online control of the incoming sensory input. Evidence suggests that sensorimotor processes may synchronize visual rhythmic activity in preparation of action performance. Indeed, we recently reported periodic fluctuations of visual contrast sensitivity that are time-locked to the onset of an intended movement of the arm. However, the origin of the observed visual modulations has so far remained unclear because of the endogenous (and thus temporally undetermined) activation of the sensorimotor system that is associated with voluntary movement initiation. In this study, we activated the sensorimotor circuitry involved in the hand control in an exogenous and controlled way by means of peripheral stimulation of the median nerve and characterized the spectrotemporal dynamics of the ensuing visual perception. The stimulation of the median nerve triggers robust and long-lasting (∼1 s) alpha-band oscillations in visual perception, whose strength is temporally modulated in a way that is consistent with the changes in alpha power described at the neurophysiological level after sensorimotor stimulation. These findings provide evidence in support of a causal role of the sensorimotor system in modulating oscillatory activity in visual areas with consequences for visual perception. NEW & NOTEWORTHY This study shows that the peripheral activation of the somatomotor hand system triggers long-lasting alpha periodicity in visual perception. This demonstrates that not only the endogenous sensorimotor processes involved in movement preparation but also the passive stimulation of the sensorimotor system can synchronize visual activity. The present work suggests that oscillation-based mechanisms may subserve core (task independent) sensorimotor integration functions.

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