Disruption of Fixation Reveals Latent Sensorimotor Processes in the Superior Colliculus

2019

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20The superior colliculus (SC) is an excellent substrate to study functional organization of 21 sensorimotor transformations. We used linear multi-contact array recordings to analyze the spatial and 22 temporal properties of population activity along the SC dorsoventral axis during delayed saccade tasks. 23During the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. 24In the ensuing delay period, the laminar organization of low-spiking rate activity matched that of the visual 25 epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, ~100ms before 26 saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and 27 ventrally, culminating in a synchronous burst across the dorsoventral axis, ~28ms before saccade onset. 28 Stimulation of individual contacts on the laminar probe produced saccades of similar vectors. Collectively, 29 the results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor 30 transformation for the control of gaze. 31 32 Introduction 33Our interactions with the environment are mediated via brain networks that transform sensory 34 signals to motor actions at the appropriate time. In the context of gaze control, this sensorimotor 35 transformation entails processing of incoming visual information and generating a movement command to 36 appropriately redirect the line of sight. The superior colliculus (SC) in the midbrain modulates its activity in 37 response to both stimulus presentation and movement generation, as well as during the interval between 38 the two events. Like cortex, the SC is composed of distinct layers. Its superficial layers are predominantly 39 driven by visual processing structures like the retina and primary visual cortex, while its deeper layers 40 communicate a broad spectrum of information with many cortical and noncortical areas [1][2][3] . It also has a 41 canonical organization with established microcircuits for communication both within and across layers 4 . 42Finally, it has a topographic representation of visual space and for generation of gaze shifts to those 43 locations 5 . Thus, the SC is ideally suited to study the neural correlates of sensorimotor transformation. 44Despite a wealth of knowledge about the anatomical organization of the SC and the functional 45 properties of individual SC neurons, current understanding about the link between structural and functional 46 organization at the population level is limited. For instance, it is unclear whether the properties of individual 47 neurons exhibit systematic spatiotemporal organization during the sensorimotor transformation, and how 48 such organization is linked to the microarchitecture of the SC network. Bridging structure with function helps 49 to not only understand the computations underlying the transformation but also to build biologically-inspired 50 network models of sensorimotor learning and behavior 6,7 . 51Linear microelectrodes...

Section: Discussionsupporting

confidence: 84%

Section: Discussionmentioning

confidence: 99%

Time-course of population activity along the dorsoventral extent of the superior colliculus during delayed saccade tasks

Massot

2019

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“…6). A related alternative explanation is that a movement is initiated specifically when movement-only neurons are active, but most neurons in sensorimotor structures like SC and FEF span a continuum between visuomovement activity and movement activity 1,34,35 . In fact, antidromically identified tectoreticular neurons that presumably drive saccade generation exhibit both visual and premotor bursts 7 .…”

Section: Perspectives On the Role Of Temporal Structurementioning

confidence: 99%

Population temporal structure supplements the rate code during sensorimotor transformations

2017

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Sensory-to-motor transformations are critically mediated by neurons in premotor brain networks whose evolving activities represent sensory, cognitive, and movement-related information. However, this multiplexing poses a conundrum: how does a decoder know precisely when to initiate a movement if such neurons are also active at times other than when a movement occurs? Extant models of movement generation that rely on firing rate, including rise-to-threshold, inhibitory gating, and dynamical switches at the population level, leave certain explanatory gaps unfilled. 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. We show that in brain regions involved in orienting eye movements - the superior colliculus and the frontal eye fields - the temporal dynamics between neurons during visually-driven activity is different from that during pre-movement activation. Specifically, using a measure that captures the fidelity of the population code, we show that the temporal structure fluctuates in the visual response but remains stable during the pre-movement response, thus distinguishing incoming sensory input from motor output. This is an important attribute because SC and FEF “visuomovement” neurons project directly to the brainstem which houses the controller for gaze shifts, and any increase in the incoming drive is poised to trigger a gaze shift. We also demonstrate that a simple firing rate-based network with synaptic facilitation can distinguish between stable and fluctuating population codes, suggesting a putative mechanism for interpreting temporal structure. These findings offer an alternative perspective on the relationship between spatial attention and motor preparation 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 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. We also used spatiotemporally patterned microstimulation to causally verify the importance of temporal structure. A spiking neuron model with dendritic integration was able to decode this temporal information. These findings offer an alternative perspective on movement generation and highlight the importance of short-term population history in neuronal communication and behaviour.

“…We would like to emphasize that the observed results -preparatory motor potential, reduced threshold, 508 accelerated activity dynamics -are most likely indirect effects of the trigeminal blink reflex, via inhibition 509 of the OPNs, and not directly due to the reflex itself. Prior work has shown that the activity of SC neurons 510 is not affected by the BREM produced during fixation (Goossens and Van Opstal, 2000a; Jagadisan and 511 Gandhi, 2016). For blinks produced after the saccade target is presented, some SC neurons in fact exhibit 512 attenuation (Goossens and Van Opstal, 2000a), although we did not see it in our dataset (and even if that 513 did happen, it is counter-intuitive to and does not explain the motor potential and acceleration of activity).…”

Section: The Role Of Sc and Brainstem In Saccade Execution 479mentioning

confidence: 99%

Removal of inhibition uncovers latent movement potential during preparation

2017

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33The motor system prepares for movements well in advance of their execution. In the gaze control system, 34 premotor neurons that produce a burst of activity for the movement are also active leading up to the 35 saccade. The dynamics of preparatory neural activity have been well described by stochastic accumulator 36 models, and variability in the accumulation dynamics has been shown to be correlated with reaction times 37 of the eventual saccade, but it is unclear whether this activity is purely preparatory in nature or has 38 features indicative of a hidden movement command. We explicitly tested whether preparatory neural 39 activity in premotor neurons of the primate superior colliculus has "motor potential". We removed 40 inhibition on the saccadic system using reflex blinks, which turn off downstream gating, and found that 41 saccades can be initiated before underlying activity reaches levels seen under normal conditions. 42Accumulating low-frequency activity was predictive of eye movement dynamics tens of milliseconds in 43 advance of the actual saccade, indicating the presence of a latent movement command. We also show that 44 reaching threshold is not a necessary condition for movement initiation, contrary to the postulates of 45 accumulation-to-threshold models. The results bring into question extant models of saccade generation 46 and support the possibility of a concurrent representation for movement preparation and generation. 47 Significance Statement 48How the brain plans for upcoming actions before deciding to initiate them is a central question in 49 neuroscience. Popular theories suggest that movement planning and execution occur in serial stages, 50 separated by a decision boundary in neural activity space (e.g., "threshold"), which needs to be crossed 51 before the movement is executed. By removing inhibitory gating on the motor system, we show here that 52 the activity required to initiate a saccade can be flexibly modulated. We also show that evolving activity 53 during movement planning is a hidden motor command. The results have important implications for our 54 understanding of how movements are generated, in addition to providing useful information for decoding 55 movement intention based on planning-related activity. 56