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

Abstract

Sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies have demonstrated saccade-related activity in the dorsal pulvinar, and we have recently shown that many neurons exhibit postsaccadic spatial preference. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (−15°, 0°, 15°) in monkeys performing a visually cued memory saccade task. We found two main types of gaze dependence. First, ~50% of neurons showed dependence on static gaze direction during initial and postsaccadic fixation, and might be signaling the position of the eyes in the orbit or coding foveal targets in a head/body/world-centered reference frame. The population-derived eye position signal lagged behind the saccade. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory, and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to postsaccadic fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in nonretinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually guided eye and limb movements. NEW & NOTEWORTHY Work on the pulvinar focused on eye-centered visuospatial representations, but position of the eyes in the orbit is also an important factor that needs to be taken into account during spatial orienting and goal-directed reaching. We show that dorsal pulvinar neurons are influenced by eye position. Gaze direction modulated ongoing firing during stable fixation, as well as visual and saccade responses to peripheral targets, suggesting involvement of the dorsal pulvinar in spatial coordinate transformations.

Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP

“…8A/B, 45, 46), insula (Romanski et al, 1997), cingulate and premotor cortices (Baleydier and Mauguiere, 1985) was expected. The effective connectivity of dPul is conceptually in line with a number of recording and lesion studies in monkeys and humans that highlight its critical contribution to higher-order visual, oculomotor and skeletomotor functions involving spatial attention (Arend et al, 2008a; Fiebelkorn et al, 2019; Karnath et al, 2002; Petersen et al, 1987; Rafal et al, 2004; Van der Stigchel et al, 2010), decision making and action selection (Dominguez-Vargas et al, 2017; Komura et al, 2013; M. Wilke et al, 2010; Wilke et al, 2013) and sensorimotor transformations for visually-guided reaching and grasping (Mundinano et al, 2018; Schneider et al, 2020; M. Wilke et al, 2010; Wilke et al, 2018, 2017). The elicited activations are also largely consistent with human studies that investigated intracerebral-evoked responses to dorso-medial pulvinar stimulation in epileptic patients (Rosenberg et al, 2009) or used fMRI functional connectivity analyses (Arcaro et al, 2018).…”

“…Based on these studies, and the predominately contralateral tuning of LIPd and dPul cue and delay period activity both on the level of single neurons and fMRI signals (Blatt et al, 1990; Caspari et al, 2015; Dominguez-Vargas et al, 2017; Fiebelkorn et al, 2019; Kagan et al, 2010; Patel et al, 2010; Schneider et al, 2020), we hypothesized that the effects of dPul and/or LIP stimulation might depend on the visual stimulation and the direction of the upcoming saccade. For instance, if microstimulation acts as a multiplicative gain mechanism we might expect the highest fMRI-elicited enhancement in the contraversive saccade task condition, at least in the stimulated hemisphere.…”

“…The dorsal pulvinar (dPul) occupies the region above the level of the brachium of the superior colliculus and encompasses the medial pulvinar (PM) and the dorsal portion of the lateral pulvinar (PLdm) (Gutierrez et al, 2000;Kaas and Lyon, 2007). Similar to LIP and vPul, dPul neurons show enhancement for visual stimuli that are attended due to their behavioral relevance and/or indicate an upcoming saccade target (Bender and Youakim, 2001;Fiebelkorn et al, 2019) and discharge in cue and saccade execution phases with an overall contralateral preference (Benevento and Port, 1995;Dominguez-Vargas et al, 2017;Robinson et al, 1986;Schneider et al, 2020). But unlike vPul and to a certain extent LIP (Patel et al, 2010), dPul does not follow a clear retinotopic organization (Benevento and Miller, 1981;Benevento and Port, 1995;Petersen et al, 1987).…”

Brain‐wide mapping of inputs to the mouse lateral posterior (LP/Pulvinar) thalamus–anterior cingulate cortex network

“…Since the SC does not project directly to ACC, the LP may serve as one of the feedback pathways for ACC-SC circuits. Multiple human and nonhuman primate studies implicate the pulvinar, SC, FEFs, and ACC together in attentional orienting (Rafal & Posner, 1987) and oculomotor functions (Schneider et al, 2020). Together with the abundance of pretectal inputs to LP→ACC neurons, it is likely that intermediate and deep layer SC inputs to medial LP in rodents are also involved in visuomotor orienting.…”

Depression and Cognitive Impairment: Current Understanding of Its Neurobiology and Diagnosis

“…Frontal memory circuits synchronized in response to stimulus presentation and memory encoding; however, they gradually desynchronized to below the baseline level over a long memory period. 106 The dorsal pulvinar in spatial coordinate transformations 107 and the mesial temporal lobe are associated with the onset of visual stimuli (image onset). 108 The intermediate layers of the SC integrate inputs from visual areas, frontal-parietal regions, and basal ganglia and project directly to the premotor circuit in the brainstem to initiate the orienting response, including not only shifts of attention and gaze but also pupil dilation.…”