Electrical Microstimulation of the Pulvinar Biases Saccade Choices and Reaction Times in a Time-Dependent Manner

Abstract

The pulvinar complex is interconnected extensively with brain regions involved in spatial processing and eye movement control. Recent inactivation studies have shown that the dorsal pulvinar (dPul) plays a role in saccade target selection; however, it remains unknown whether it exerts effects on visual processing or at planning/execution stages. We used electrical microstimulation of the dPul while monkeys performed saccade tasks toward instructed and freely chosen targets. Timing of stimulation was varied, starting before, at, or after onset of target(s). Stimulation affected saccade properties and target selection in a time-dependent manner. Stimulation starting before but overlapping with target onset shortened saccadic reaction times (RTs) for ipsiversive (to the stimulation site) target locations, whereas stimulation starting at and after target onset caused systematic delays for both ipsiversive and contraversive locations. Similarly, stimulation starting before the onset of bilateral targets increased ipsiversive target choices, whereas stimulation after target onset increased contraversive choices. Properties of dPul neurons and stimulation effects were consistent with an overall contraversive drive, with varying outcomes contingent upon behavioral demands. RT and choice effects were largely congruent in the visually-guided task, but stimulation during memory-guided saccades, while influencing RTs and errors, did not affect choice behavior. Together, these results show that the dPul plays a primary role in action planning as opposed to visual processing, that it exerts its strongest influence on spatial choices when decision and action are temporally close, and that this choice effect can be dissociated from motor effects on saccade initiation and execution.SIGNIFICANCE STATEMENT Despite a recent surge of interest, the core function of the pulvinar, the largest thalamic complex in primates, remains elusive. This understanding is crucial given the central role of the pulvinar in current theories of integrative brain functions supporting cognition and goal-directed behaviors, but electrophysiological and causal interference studies of dorsal pulvinar (dPul) are rare. Building on our previous studies that pharmacologically suppressed dPul activity for several hours, here we used transient electrical microstimulation at different periods while monkeys performed instructed and choice eye movement tasks, to determine time-specific contributions of pulvinar to saccade generation and decision making. We show that stimulation effects depend on timing and behavioral state and that effects on choices can be dissociated from motor effects.

The mouse pulvinar nucleus: Organization of the tectorecipient zones

“…Additionally, although the pulvinar is commonly considered a single thalamic nucleus, it contains a number of distinct subregions which may be differentially involved in the various functions ascribed to the pulvinar (e.g. visual attention, decision making, motor planning, perceptual suppression, synchronization of cortical activity, detection of faces or fearful stimuli; Dominguez-Vargas et al, 2017; Grimaldi et al, 2016; Van Le et al, 2014; Le et al, 2014, 2016; McFadyen et al, 2017; Soares et al, 2017; Wilke et al, 2009, 2010, 2013; Zhou et al, 2016). In order to understand how the pulvinar contributes to these various tasks, the synaptic circuits within each subregion must first be defined.…”

Development of a monkey avatar to study social perception in macaques

“…All animals had been previously implanted with cranial plastic "headposts" under general anaesthesia and aseptic conditions, for participating in neurophysiological experiments. The surgical procedures and purpose of these implants were described previously in detail (22). Monkeys were previously trained in both using the primate chair, and in fixating their gaze for eye tracking calibration.…”

Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

“…enhancement for visual stimuli that indicate an upcoming saccade target (Robinson, 1993). While the dorsal pulvinar is not retinotopically organized and its neurons have large receptive fields, they discharge in the context of saccade tasks in visual cue and saccade execution phases, exhibiting overall preference for contralateral visual cue, peri-and post-saccadic responses (Petersen et al, 1985;Benevento and Port, 1995;Dominguez-Vargas et al, 2017).…”

“…In contrast to primary oculomotor regions (e.g. SC, FEF or internal medullary lamina (IML)/central thalamus (Schiller and Tehovnik, 2005;Tanaka and Kunimatsu, 2011)), relatively high currents (>150 µA) are necessary to evoke saccades and those are small, infrequent and might depend on behavioral context (Dominguez-Vargas et al, 2017). Apart from eye movement selection, the dorsal pulvinar also plays a critical role in other visuomotor behaviors such as reaching and grasping; its neural activity correlates with reach movements (Cudeiro et al, 1989;Acuna et al, 1990) and inactivation/lesions in monkeys and humans lead to hand-and space-specific deficits in reach and grasp tasks (Wilke et al, 2010(Wilke et al, , 2018.…”

“…In fact, very basic questions such as whether dorsal pulvinar neurons carry eye position signals and how those interact with visual cue responses have not been addressed. Even the effect of static eye position on ongoing firing has not been tested, although the presence of tonic firing during initial and post-saccadic fixation (Dominguez-Vargas et al, 2017) as well as nystagmus and smooth pursuit deficits following dorsal pulvinar inactivation/lesions suggest that it might be involved in gaze stabilization as well (Ohtsuka et al, 1991;Wilke et al, 2010Wilke et al, , 2018.…”