Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

Abstract

22At any moment in time, new information is sampled from the environment and interacts with 23 ongoing brain state. Often, such interaction takes place within individual circuits that are 24 capable of both mediating the internally ongoing plan as well as representing exogenous 25 sensory events. Here we investigated how sensory-driven neural activity can be integrated, 26 very often in the same neuron types, into ongoing oculomotor commands for saccades. 27Despite the ballistic nature of saccades, visually-induced action potentials in the superior 28 colliculus (SC), a structure known to drive eye movements, not only occurred intra-29 saccadically, but they were also associated with highly predictable modifications of the 30 ongoing eye movements. Such modifications were also possible by peri-saccadically 31 injecting single, double, or triple electrical microstimulation pulses into the SC. Our results 32 suggest instantaneous readout of the SC map during movement generation, irrespective of 33 activity source, and explain a significant component of kinematic variability of motor outputs. 34 35 question is important to clarify mechanisms of readout from circuits in which functional 62 multiplexing is prevalent. 63In the SC, our focus here, there have been many debates about how this structure 64 contributes to saccade control (Waitzman et al., 1991;Ivan et al., 2018). In recent proposals 65 (Goossens and Van Opstal, 2006;Van Opstal and Goossens, 2008; Goossens and Van 66 Opstal, 2012), it was suggested that every spike emitted by SC neurons during their "motor" 67 bursts contributes a mini-vector of movement tendency, such that the aggregate sum of all 68 output spikes is read out by downstream structures to result in a given movement trajectory. 69However, implicit in these models is the assumption that only action potentials within a 70 narrow time window around movement triggering (the "motor" burst) matter. Any other 71 spiking, by the same or other neurons, before or after the eye movement is irrelevant. This 72 causes a significant readout problem, since downstream neurons do not necessarily have 73 the privilege of knowing which spikes should now count for a given eye movement 74 implementation and which not. 75Indeed, from an ecological perspective, an important reason for multiplexing could be 76 exactly to maintain flexibility to rapidly react to the outside world, even in a late motor control 77 structure. In that sense, rather than invoking mechanisms that allow actively ignoring "other 78 spiking" activity outside of the currently triggered eye movement (whether spatially or 79 temporally), one would predict that SC readout, at any one moment, should be quite 80 sensitive to any spiking activity regardless of its source. We experimentally tested this 81 hypothesis. We "injected" SC spiking activity around the time of saccade generation, but at 82 a spatially dissociated location. We uncovered causal evidence that the entire landscape of 83 SC activity can instantaneously contribute to individual ...

Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements

“…A further implication of the results of SC inactivation on early cue-influenced microsaccade directions ( Figure 3 ) is that one can now attempt to establish a quantitative link between microsaccade endpoint variability and SC cue-induced visual bursts. Specifically, the timing of early cue-congruent microsaccades in Figures 1 – 3 is consistent with the timing of SC visual bursts ( Buonocore et al, 2017 , 2020b ). If eliminating such visual bursts via SC inactivation diminishes the likelihood of cue-congruent microsaccades ( Figure 3 ; Hafed et al, 2013 ), then this might suggest that these cue-congruent microsaccades reflect readout of the SC map under a very specific simultaneity condition: a microsaccade burst in the direction of the appearing cue in the rostral SC region, and a simultaneous visual burst in the periphery at the site representing the cue’s location ( Figure 5A ).…”

“…If eliminating such visual bursts via SC inactivation diminishes the likelihood of cue-congruent microsaccades ( Figure 3 ; Hafed et al, 2013 ), then this might suggest that these cue-congruent microsaccades reflect readout of the SC map under a very specific simultaneity condition: a microsaccade burst in the direction of the appearing cue in the rostral SC region, and a simultaneous visual burst in the periphery at the site representing the cue’s location ( Figure 5A ). If true, then there should be a measurable number of cue-induced visual spikes that are “injected” onto the SC map (when the cue appears) at the same time as the triggering of microsaccades ( Buonocore et al, 2017 , 2020b ). This should “add” to the triggered movements and alter their size.…”

“…Thus, every spike of every active cue-driven SC neuron contributes to microsaccade endpoint variability. Adapted with permission from Buonocore et al (2020b) .…”

“…This idea was validated by measuring early cue-congruent microsaccade metrics: cue-congruent microsaccades were significantly larger in size than other microsaccades ( Hafed and Ignashchenkova, 2013 ; Tian et al, 2016 ; Buonocore et al, 2020b ). Importantly, there was also a quantitatively predictable relationship between the number of cue-induced visual spikes in the peripheral SC and the cue-congruent microsaccade amplitudes.…”

“…Importantly, there was also a quantitatively predictable relationship between the number of cue-induced visual spikes in the peripheral SC and the cue-congruent microsaccade amplitudes. To demonstrate this, Buonocore et al (2020b) counted the number of visual spikes emitted by individually recorded peripheral SC neurons at the time of microsaccade triggering ( Figure 5A ). There was a linear relationship between the number of peripheral “visual” spikes and cue-congruent microsaccade amplitudes ( Figures 5B,C ): every single spike of every single visually-driven neuron contributed to the trajectory of early cue-congruent microsaccades ( Buonocore et al, 2020b ).…”