Dynamic pulvino-cortical interactions in the primate attention network

Kästner, Sabine; Fiebelkorn, Ian C.; Eradath, Manoj K.

doi:10.1016/j.conb.2020.08.002

Cited by 39 publications

(27 citation statements)

References 83 publications

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“…It has been suggested that these cortico-TC loops form indirect (transthalamic) pathways through which the pulvinar may influence cortical processing (Kastner & Ungerleider, 2000;Gutierrez et al, 2000;Adams et al, 2000;Shipp, 2001;Shipp, 2003;Gattass et al, 2014;Arcaro, Pinsk, & Kastner, 2015;Jaramillo et al, 2019;reviewed in Buschman & Kastner, 2015;. In line with the cortico-TC loop hypothesis, electrophysiological studies have shown that the transthalamic pathways serve to regulate information transmission between interconnected cortical areas Halassa & Kastner, 2017;Kastner et al, 2020;Saalmann et al, 2012). Specifically, during selective visual attention, the pulvinar synchronizes neural activity between interconnected cortical areas in the alpha/low beta frequency range (8-15 Hz), as shown for visual areas V4 and TEO (Saalmann et al, 2012), the lateral intraparietal area (LIP) and V4 (Saalmann et al, 2018), and LIP and FEF .…”

Section: Antibody Namementioning

confidence: 95%

A causal role for the pulvinar in coordinating task‐independent cortico–cortical interactions

Eradath

Pinsk

Kästner

2021

J of Comparative Neurology

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The pulvinar is the largest nucleus in the primate thalamus and has topographically organized connections with multiple cortical areas, thereby forming extensive cortico-pulvino-cortical input-output loops. Neurophysiological studies have suggested a role for these transthalamic pathways in regulating information transmission between cortical areas. However, evidence for a causal role of the pulvinar in regulating cortico-cortical interactions is sparse and it is not known whether pulvinar's influences on cortical networks are task-dependent or, alternatively, reflect more basic large-scale network properties that maintain functional connectivity across networks regardless of active task demands. In the current study, under passive viewing conditions, we conducted simultaneous electrophysiological recordings from ventral (area V4) and dorsal (lateral intraparietal area [LIP]) nodes of macaque visual system, while reversibly inactivating the dorsal part of the lateral pulvinar (dPL), which shares common anatomical connectivity with V4 and LIP, to probe a causal role of the pulvinar. Our results show a significant reduction in local field potential phase coherence between LIP and V4 in low frequencies (4-15 Hz) following muscimol injection into dPL. At the local level, no significant changes in firing rates or LFP power were observed in LIP or in V4 following dPL inactivation. Synchronization between pulvinar spikes and cortical LFP phase decreased in low frequencies (4-15 Hz) both in LIP and V4, while the low frequency synchronization between LIP spikes and pulvinar phase increased. These results indicate a causal role for pulvinar in synchronizing neural activity between interconnected cortical nodes of a large-scale network, even in the absence of an active task state.

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Section: Antibody Namementioning

confidence: 95%

A causal role for the pulvinar in coordinating task‐independent cortico–cortical interactions

Eradath

Pinsk

Kästner

2021

J of Comparative Neurology

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“…Although the co-activation along the STS elicited by pulvinar and LIP stimulation was not specific for face patches, we speculate that this shared connectivity might facilitate attention to faces by routing information from early visual areas to IT cortex and/or help to filter the important (e.g. facial) information from behaviorally irrelevant features (Bridge et al, 2015; Hesse and Tsao, 2020; Kastner et al, 2020). These data are also compatible with the notion of pulvinar involvement in face processing and social cognition, e.g.…”

Section: Discussionmentioning

confidence: 84%

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

Kagan

Gibson

Spanou

et al. 2020

Preprint

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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.HighlightsElectrical stimulation of pulvinar and LIP was used to study fMRI effective connectivityBoth regions activated prefrontal cortex and the dorsal bank of superior temporal sulcusActivations within and across hemispheres suggest polysynaptic propagationStimulation effects show interactions between task- and spatial selectivityStimulation effects are best fitted by an additive model scaled by the initial response

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“…The rodent homolog of the primate pulvinar, the lateral posterior (LP) thalamic nucleus, is a higher order visual thalamic structure that shares reciprocal connectivity with multiple visual, associational, and frontal cortical areas (Adams et al., 2000; Juavinett et al., 2019; Scholl et al., 2020). The pulvinar/LP has been implicated in a broad range of functions that extend beyond visual processing, including conveying saccade‐related activity, coordinating visually guided movements, and mediating spatial attention (Kaas & Lyon, 2007; Kastner et al., 2020; Robinson et al., 1986). Like the primate pulvinar, rodent LP is organized into different subregions, each with preferential inputs from distinct subcortical and cortical areas along the visual hierarchy (Bennett et al., 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Medial pulvinar connections with frontal and premotor areas are likely involved in higher order visual cognition rather than early visual processing (Homman‐Ludiye & Bourne, 2019; Homman‐Ludiye & Bourne, 2021; Romanski et al., 1997). Mutual interactions between the pulvinar and the frontal‐parietal attention network regulate sustained and selective attentional allocation during visual decision making (Rafal & Posner, 1987; Snow et al., 2020; Kastner et al., 2020). Lesions or inactivation of the primate dorsal/medial pulvinar appear to impair visual decision making, but performance in visual tasks remains intact following manipulations to the tasks' incentive structure and presumably attentional allocation (Komura et al., 2013; Wilke et al., 2013), suggesting that inactivating medial pulvinar does not impair simple visual processing.…”

Section: Introductionmentioning

confidence: 99%

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

Leow

Zhou

Sullivan

et al. 2022

J of Comparative Neurology

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The rodent homolog of the primate pulvinar, the lateral posterior (LP) thalamus, is extensively interconnected with multiple cortical areas. While these cortical interactions can span the entire LP, subdivisions of the LP are characterized by differential connections with specific cortical regions. In particular, the medial LP has reciprocal connections with frontoparietal cortical areas, including the anterior cingulate cortex (ACC). The ACC plays an integral role in top-down sensory processing and attentional regulation, likely exerting some of these functions via the LP. However, little is known about how ACC and LP interact, and about the information potentially integrated in this reciprocal network. Here, we address this gap by employing a projectionspecific monosynaptic rabies tracing strategy to delineate brain-wide inputs to bottomup LP→ACC and top-down ACC→LP neurons. We find that LP→ACC neurons receive inputs from widespread cortical regions, including primary and higher order sensory and motor cortical areas. LP→ACC neurons also receive extensive subcortical inputs, particularly from the intermediate and deep layers of the superior colliculus (SC).Sensory inputs to ACC→LP neurons largely arise from visual cortical areas. In addition, ACC→LP neurons integrate cross-hemispheric prefrontal cortex inputs as well as inputs from higher order medial cortex. Our brain-wide anatomical mapping of inputs to the reciprocal LP-ACC pathways provides a roadmap for understanding how LP and ACC communicate different sources of information to mediate attentional control and visuomotor functions.

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Dynamic pulvino-cortical interactions in the primate attention network

Cited by 39 publications

References 83 publications

A causal role for the pulvinar in coordinating task‐independent cortico–cortical interactions

A causal role for the pulvinar in coordinating task‐independent cortico–cortical interactions

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

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

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