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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 demonstrated saccade-related ac...
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... also asked, more generally, if the units with the initial gaze effect were less likely to have visual cue responses. Table 2 shows that it was not the case: units with and without an effect of initial gaze position exhibited similar cue response patterns. ...Citations
... In contrast, the dorsal pulvinar-comprising the PLdm and PM-aligns more with higher-order cognitive processes [21]. It is functionally connected to the frontal, parietal, and cingulate cortices and plays a critical role in attentional control, such as goal-directed eye movements, and other complex cognitive functions [26,37,55]. Particularly, the PM processes fear-eliciting stimuli, such as images of snakes, through its connections with the amygdala [45,[56][57][58][59]. ...
The pulvinar nucleus, a substantial and heterogeneous structure within the thalamus, plays a crucial role in modulating and coordinating cortical activities. Despite its importance, the precise mechanisms underlying the pulvinar's impact on cognitive functions remain unclear. This literature review investigates the role of the pulvinar in integrating and segregating cortical networks during complex cognitive tasks. We explore its involvement in neuronal processes like visual salience, selection, attention regulation, and the integration of sensory information and feature binding. Additionally, we discuss how impairments in these cognitive functions can profoundly impact mental health disorders, such as schizophrenia, autism spectrum disorders, depression, and anxiety. In doing so, we aim to establish coherence with theoretical frameworks, examining the pulvinar's potential roles in signal modulation across the cortical network. This analysis is framed within the contexts of the global neuronal workspace theory and predictive coding, providing a structured approach to understanding the contributions of these mechanisms to cognitive deficits. In addition, we explore how this modulation could indirectly influence other brain structures, like the amygdala, involved in emotional processing and memory consolidation, highlighting a potential connection between cognitive and emotional integration within these systems. Insights from this review could enrich our understanding of how the pulvinar modulates neural activities and contributes to our comprehension of the sources of cognitive deficits.
... /2024 suppression following saccades, that initiated by the activation of inhibitory neurons in layer IV in area V4. The authors suggested the Pulvinar as a possible neural source for this response, which was previously suggested to carry CD signal from the SC to various visual areas such as MT in primates and V1 in rodents and primates (Stepniewska et al., 2000;Shipp, 2004;Berman and Wurtz, 2010;Kuang et al., 2012;Schneider et al., 2020Schneider et al., , 2023Miura and Scanziani, 2022). Therefore, the initial suppression phase we report can fit to a similar possible pathway from the SC through the Pulvinar into the inhibitory neurons in V1. ...
Our eyes are never still. Even when we attempt to fixate, the visual gaze is never motionless, as we continuously perform miniature oculomotor movements termed as fixational eye movements. The fastest eye movements during the fixation epochs are termed microsaccades (MSs), that are leading to continual motion of the visual input, affecting mainly neurons in the fovea. Yet our vision appears to be stable. To explain this gap, previous studies suggested the existence of an extra-retinal input (ERI) into the visual cortex that can account for the motion and produce visual stability. Here, we investigated the existence of an ERI to V1 fovea in behaving monkeys while they performed spontaneous MSs, during fixation. We used voltage-sensitive dye imaging (VSDI) to measure and characterize at high spatio-temporal resolution the influence of MSs on neural population activity, in the foveal region of the primary visual cortex (V1). In the absence of a visual stimulus, MSs induced a two-phase response modulation: an early suppression transient followed by an enhancement transient. A correlation analysis revealed an increase in neural synchronization around ~100 ms after MS onset. Next, we investigated the MS effects in the presence of a small visual stimulus, and found that this modulation was different from the non-stimulated condition yet both modulations co-existed in the fovea. Finally, the VSD response to an external motion of the fixation point could not explain the MS modulation. These results support an ERI that may be involved in visual stabilization already at the level of V1.
... In sum, the results of these experiments confirm the prediction from neural models 30 that eye movements participate in shaping visual sensitivity. This action stems directly from the consequences of eye movements for visual input signals, rather than their associated extraretinal influences [41][42][43][44][45] : by regulating the extent by which luminance modulations fall within the temporal bandwidth of the visual system, the fixational motion of the eye effectively controls the contrast of the stimulus on the retina. Contrary to the traditional notion of a non-specific gain resulting from a global "refreshing" of neural activity, this modulation is not uniform across spatial frequencies, but it respectively enhances sensitivity to lower and higher spatial frequencies when the amount of motion increases or decreases. ...
... Such inactivation-induced bias could be alleviated by presenting only a single target or increasing the reward for contralesional targets but less so by perceptual saliency manipulations 27 . The above causal perturbation findings, and the results of electrophysiological recordings [29][30][31][32][33][34][35] , on the one hand, implicate dPul in attentional allocation for perceptual processing, but on the other, are also compatible with a role in more general spatial orienting and selection bias. Different task demands might be one reason for such interpretational ambiguity. ...
The dorsal pulvinar has been implicated in visuospatial attentional and perceptual confidence processing. Pulvinar lesions in humans and monkeys lead to spatial neglect symptoms, including an overt spatial saccade bias during free choices. However, it remains unclear whether disrupting the dorsal pulvinar during target selection that relies on a perceptual decision leads to a perceptual impairment or a more general spatial orienting and choice deficit. To address this question, we reversibly inactivated the unilateral dorsal pulvinar by injecting GABA-A agonist THIP while two macaque monkeys performed a color discrimination saccade task with varying perceptual difficulty. We used Signal Detection Theory and simulations to dissociate perceptual sensitivity (d-prime) and spatial selection bias (response criterion) effects. We expected a decrease in d-prime if dorsal pulvinar affects perceptual discrimination and a shift in response criterion if dorsal pulvinar is mainly involved in spatial orienting. After the inactivation, we observed response criterion shifts away from contralesional stimuli, especially when two competing stimuli in opposite hemifields were present. Notably, the d-prime and overall accuracy remained largely unaffected. Our results underline the critical contribution of the dorsal pulvinar to spatial orienting and action selection while showing it to be less important for visual perceptual discrimination.
... Conversely, the dorsal pulvinar of primates, consisting of the PLdm and PM, aligns more with higher-order cognitive processes [16]. It is functionally connected to frontal, parietal, and cingulate cortices and is essential for attentional control (e.g., goal-directed eye movements) and other advanced cognitive functions [14,16,35]. For example, dorsal pulvinar, like PM, processes fear-eliciting stimuli like images of snakes through its connectivity with the amygdala [36,37]. ...
The pulvinar nucleus of the thalamus is a crucial component of the visual system and plays significant roles in sensory processing and cognitive integration. The pulvinar’s extensive connectivity with cortical regions allows for bidirectional communication, contributing to the integration of sensory information across the visual hierarchy. Recent findings underscore the pulvinar’s involvement in attentional modulation, feature binding, and predictive coding. In this review, we highlight recent advances in clarifying the pulvinar’s circuitry and function. We discuss the contributions of the pulvinar to signal modulation across the global cortical network and place these findings within theoretical frameworks of cortical processing, particularly the global neuronal workspace (GNW) theory and predictive coding.
... Moreover, the medial pulvinar is connected to several brain regions, such as the amygdala, hippocampus, temporal neocortex, cingulate, and orbitofrontal cortex. It has been observed that pulvinar units become active in response to movements, auditory stimuli, visual stimuli, and even list stimuli, such as letters and numbers (Magariños-Ascone et al., 1988;Schneider et al., 2020), highlighting the importance of pulvinar activity in the processing of sensory information. ...
... In response to movements, auditory stimuli, or visual stimuli, pulvinar units activate (Magariños-Ascone et al., 1988). Moreover, recent research has also suggested that the pulvinar is involved in processing list stimuli, such as letters and numbers, as pulvinar activity has been observed in response to these stimuli (Schneider et al., 2020). This indicates that the pulvinar's role in sensory processing extends beyond traditional visual and auditory stimuli. ...
The role of thalamocortical circuits in memory has driven a recent burst of scholarship, especially in animal models. Investigating this circuitry in humans is more challenging. And yet, the development of new recording and stimulation technologies deployed for clinical indications has created novel opportunities for data collection to elucidate the cognitive roles of thalamic structures. These technologies include stereoelectroencephalography (SEEG), deep brain stimulation (DBS), and responsive neurostimulation (RNS), all of which have been applied to memory-related thalamic regions, specifically for seizure localization and treatment. This review seeks to summarize the existing applications of neuromodulation of the anterior thalamic nuclei (ANT) and highlight several devices and their capabilities that can allow cognitive researchers to design experiments to assay its functionality. Our goal is to introduce to investigators, who may not be familiar with these clinical devices, the capabilities, and limitations of these tools for understanding the neurophysiology of the ANT as it pertains to memory and other behaviors. We also briefly cover the targeting of other thalamic regions including the centromedian (CM) nucleus, dorsomedial (DM) nucleus, and pulvinar, with associated potential avenues of experimentation.
... The above causal perturbation findings, and the results of electrophysiological recordings (Robinson and Petersen, 1992;Benevento and Port, 1995;Bender and Youakim, 2001;Dominguez-Vargas et al., 2017;Fiebelkorn et al., 2019;Schneider et al., 2019Schneider et al., , 2021, on the one hand, implicate dPul in attentional allocation and perceptual processing, but on the other, are also compatible with a role in more general spatial orienting bias. Different task demands might be one reason for such interpretational ambiguity. ...
Dorsal pulvinar has been implicated in visuospatial attentional and perceptual confidence processing. Perturbations of the dorsal pulvinar also induce an overt spatial saccade bias during free choices. But it remains unclear whether the dorsal pulvinar inactivation during an oculomotor target selection based on a perceptual decision will lead to perceptual impairment or a more general orienting deficit. To address this question, we reversibly inactivated unilateral dorsal pulvinar by injecting GABA-A agonist THIP while two macaque monkeys performed a color discrimination saccade response task with varying perceptual difficulty. We used Signal Detection Theory to dissociate perceptual discrimination (dprime) and spatial selection bias (response criterion) effects. We expected a decrease in dprime if dorsal pulvinar affects perceptual discrimination and a shift in response criterion if dorsal pulvinar is mainly involved in spatial orienting. After inactivation, we observed response criterion shifts away from contralesional stimuli, especially when two competing peripheral stimuli in opposite hemifields were present, for both difficulty levels. The saccade latency for the contralesional selection increased under all conditions. Notably, the dprime and overall accuracy remained largely unaffected. Our results underline the critical contribution of the dorsal pulvinar to spatial orienting while being less important for perceptual discrimination.
... The authors suggested that only when the stimulus serves as an immediate saccade target the visual response takes place, although it is not the pattern typically observed in the frontoparietal cortical areas. Finally, we recently have shown that dPul neurons carry information about static eye position and combine spatial encoding in eye-centered and nonretinocentric coordinates, potentially contributing to coordinate frame transformations (Schneider et al. 2019). ...
... The notable exception is a study that covered both lateral and medial parts of the dorsal pulvinar, predominantly at the border between the two (Benevento and Port 1995). Our recording sites were largely within the medial pulvinar (MPul) or around the border between the medial and the lateral pulvinar (see also (Dominguez-Vargas et al. 2017;Schneider et al. 2019)). We did not observe any clear patterns along the dorsal/lateralventral/medial axis in the features we tested, and such patterns have also not been reported in the previous work. ...
... Potentially, deviations of the post-saccadic eye position from the intended target location, i.e. error signals, could also be encoded in post-saccadic responses, as has been found in LIP (Zhou, Liu, et al. 2016;Munuera and Duhamel 2020), but the small saccade endpoint dispersion due to fairly stereotypical movements in our experiment did not allow to systematically check for this possibility. Finally, the spatially-tuned post-saccadic responses could also signal the new gaze position, alone or in a combination with previous eye movement vector or pre-saccadic position, and utilized for internal monitoring during action sequences (Genovesio et al. 2007;Tanaka 2007;Schneider et al. 2019). ...
Causal perturbation studies suggest that the primate dorsal pulvinar (dPul) plays a crucial role in target selection and saccade planning, but many of its basic visuomotor neuronal properties are unclear. While some functional aspects of dPul and interconnected frontoparietal areas - such as ipsilesional choice bias after inactivation - are similar, it is not known if dPul neurons share oculomotor response properties of cortical circuitry. In particular, the delay period and choice-related activity have not been explored. Here we investigated visuomotor timing and tuning in macaque dPul during instructed and free choice memory saccades using electrophysiological recordings. Most units (80%) showed significant visual (16%), visuomotor (29%) or motor-related (35%) responses. Visual cue responses were mainly contralaterally-tuned; motor responses showed weak contralateral bias. Saccade-related responses (enhancement and suppression) were more common (64%) than cue-driven responses (45%). Pre-saccadic enhancement was less frequent (9-15% depending on the definition), and only few units exhibited classical visuomotor patterns such as a combination of cue and continuous delay period activity up to the saccade onset, or pre-saccadic ramping. Instead, activity was often suppressed during movement planning (30%) and execution phases (19%). Interestingly, most spatially-selective neurons did not encode the upcoming decision during the delay in free choice trials. Thus, in absence of a visible goal, the dorsal pulvinar has only a limited role in the prospective motor planning, with response patterns partially complementary to its frontoparietal cortical partners. Conversely, prevalent cue and post-saccadic responses imply that the dorsal pulvinar participates in integrating spatial goals with processing across saccades.
... This is in agreement with the marked somatosensory properties of this part of the pulvinar. It coincides with the already discussed evidence that medio-dorsal damage to the pulvinar leads to postural deficits, possibly of proprioceptive origin (Wilke et al., 2018) and that the dorsal pulvinar contributes to the maintenance of gaze during postural changes (Schneider et al., 2019). ...
Perception in ambiguous environments relies on the combination of sensory information from various sources. Most associative and primary sensory cortical areas are involved in this multisensory active integration process. As a result, the entire cortex appears as heavily multisensory. In this review, we focus on the contribution of the pulvinar to multisensory integration. This subcortical thalamic nucleus plays a central role in visual detection and selection at a fast time scale, as well as in the regulation of visual processes, at a much slower time scale. However, the pulvinar is also densely connected to cortical areas involved in multisensory integration. In spite of this, little is known about its multisensory properties and its contribution to multisensory perception. Here, we review the anatomical and functional organization of multisensory input to the pulvinar. We describe how visual, auditory, somatosensory, pain, proprioceptive and olfactory projections are differentially organized across the main subdivisions of the pulvinar and we show that topography is central to the organization of this complex nucleus. We propose that the pulvinar combines multiple sources of sensory information to enhance fast responses to the environment, while also playing the role of a general regulation hub for adaptive and flexible cognition.
... 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). ...
... 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 thalamic pulvinar and the lateral intraparietal area (LIP) share reciprocal anatomical connections and are part of an extensive cortical and subcortical network involved in spatial attention and oculomotor processing. The goal of this study was to compare the effective connectivity of dorsal pulvinar (dPul) and LIP and to probe the dependency of microstimulation effects on task demands and spatial tuning properties of a given brain region. To this end, we applied unilateral electrical microstimulation in the dPul and LIP in combination with event-related BOLD fMRI in monkeys performing fixation and memory-guided saccade tasks. Microstimulation in both dPul and LIP enhanced task-related activity in monosynaptically-connected prefrontal cortex and along the superior temporal sulcus (STS) as well as in extrastriate cortex. Both dPul and LIP stimulation also elicited activity in several cortical areas in the opposite hemisphere, implying polysynaptic propagation of excitation. LIP microstimulation elicited strong activity in the opposite homotopic LIP while no homotopic activation was found during dPul stimulation. Despite extensive activation along the intraparietal sulcus evoked by LIP stimulation, there was a difference in frontal and occipital connectivity elicited by posterior and anterior LIP stimulation sites. Comparison of dPul stimulation with the adjacent but functionally distinct ventral pulvinar also showed distinct connectivity. On the level of single trial timecourses within a region, most microstimulation regions did not show task-dependence of stimulation-elicited response modulation. Across regions, however, there was an interaction between the task and the stimulation, and task-specific correlations between the initial spatial selectivity and the magnitude of stimulation effect were observed. Consequently, stimulation-elicited modulation of task-related activity was best fitted by an additive model scaled down by the initial response amplitude. In summary, we identified overlapping and distinct patterns of thalamocortical and corticocortical connectivity of the two key visuospatial areas, highlighting the dorsal bank and fundus of STS as a prominent node of shared circuitry. Spatial task-specific and partly polysynaptic modulations of cue and saccade planning delay period activity in both hemispheres exerted by unilateral pulvinar and parietal stimulation provide insight into the distributed interhemispheric processing underlying spatial behavior.
Highlights
Electrical stimulation of pulvinar and LIP was used to study fMRI effective connectivity
Both regions activated prefrontal cortex and the dorsal bank of superior temporal sulcus
Activations within and across hemispheres suggest polysynaptic propagation
Stimulation effects show interactions between task- and spatial selectivity
Stimulation effects are best fitted by an additive model scaled by the initial response
