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

Kagan, Igor; Gibson, Lydia; Spanou, Elena; Wilke, Melanie

doi:10.1101/2020.09.16.298539

Cited by 5 publications

(12 citation statements)

References 143 publications

(354 reference statements)

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“…In addition, the pulvinar is likely to influence the dorsal stream of visual processing (Milner & Goodale, 1995;Ungerleider & Mishkin, 1982), given its reciprocal connections with the lateral intraparietal cortex (Kagan et al, 2021) and its identified contributions to visuospatial attentional task processing, decision-making and multisensory integration (Froesel et al, 2021;Komura et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Cortico‐thalamocortical interactions for learning, memory and decision‐making

Perry

Méndez

Mitchell

2022

The Journal of Physiology

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The thalamus and cortex are interconnected both functionally and anatomically and share a common developmental trajectory. Interactions between the mediodorsal thalamus (MD) and different parts of the prefrontal cortex are essential in cognitive processes, such as learning and adaptive decision‐making. Cortico‐thalamocortical interactions involving other dorsal thalamic nuclei, including the anterior thalamus and pulvinar, also influence these cognitive processes. Our work, and that of others, indicates a crucial influence of these interdependent cortico‐thalamocortical neural networks that contributes actively to the processing of information within the cortex. Each of these thalamic nuclei also receives potent subcortical inputs that are likely to provide additional influences on their regulation of cortical activity. Here, we highlight our current neuroscientific research aimed at establishing when cortico‐MD thalamocortical neural network communication is vital within the context of a rapid learning and memory discrimination task. We are collecting evidence of MD–prefrontal cortex neural network communication in awake, behaving male rhesus macaques. Given the prevailing evidence, further studies are needed to identify both broad and specific mechanisms that govern how the MD, anterior thalamus and pulvinar cortico‐thalamocortical interactions support learning, memory and decision‐making. Current evidence shows that the MD (and the anterior thalamus) are crucial for frontotemporal communication, and the pulvinar is crucial for frontoparietal communication. Such work is crucial to advance our understanding of the neuroanatomical and physiological bases of these brain functions in humans. In turn, this might offer avenues to develop effective treatment strategies to improve the cognitive deficits often observed in many debilitating neurological disorders and diseases and in neurodegeneration.

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Section: Discussionmentioning

confidence: 99%

Cortico‐thalamocortical interactions for learning, memory and decision‐making

Perry

Méndez

Mitchell

2022

The Journal of Physiology

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“…When comparing results presented in the current work with the few previous studies on visual and oculomotor motor properties of the pulvinar, it is important to note that most studies in the dorsal pulvinar recorded from the dorsomedial division of the lateral pulvinar. This division is currently denoted as PLdm (Kaas and Lyon 2007; Bridge et al 2015; Kagan et al 2021), or as Pdm in original electrophysiological studies by Robinson, Petersen and colleagues, e.g. (Petersen et al 1985, 1987; Robinson et al 1986; Bender and Youakim 2001).…”

Section: Discussionmentioning

confidence: 99%

“…The guide tube was filled with sterile silicone oil prior to electrode insertion, to ensure smooth electrode travel and to prevent the backflow of cerebrospinal fluid. T1- and T2-weighted scans were co-registered and transformed into “chamber normal” (aligned to the chamber vertical axis) and to anterior commissure – posterior commissure (AC-PC) space for electrode targeting and visualization in BrainVoyagerQX (Brain Innovation, Netherlands) and Planner (Ohayon and Tsao 2012; Kagan et al 2021).…”

Section: Methodsmentioning

confidence: 99%

“…Distinct pulvinar subdivisions might however contribute differently to these functions. Several studies have motivated a functional distinction between the ventral and the dorsal pulvinar aspects, based either on distinctive patterns of anatomical (Stepniewska et al 1994;Kaas and Lyon 2007) and functional/effective connectivity (Arcaro et al 2015(Arcaro et al , 2018Kagan et al 2021), or based on dissimilar functional properties within the same anatomically-defined subdivision, e.g. leading to further division of the lateral pulvinar into dorsal and ventral parts (Petersen et al 1985;Baldwin et al 2017).…”

Section: Introductionmentioning

confidence: 99%

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Visual, delay and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

Schneider

Dominguez-Vargas

Gibson

et al. 2021

Preprint

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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.

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“…These nuclei developed together with the association cortices in the course of primate evolution and are reciprocally connected to the parietal and prefrontal cortex, orbitofrontal cortex, insula, cingulate, superior and inferior temporal cortex (Kaas and Lyon, 2007; Preuss, 2007; Kaas and Baldwin, 2020). This extensive connectivity profile identifies the dorsal pulvinar as a unique brain hub well situated to interact with and modulate the circuitry involved in spatial attentional orienting and target selection (Grieve et al, 2000; Sherman and Guillery, 2002; Shipp, 2003; Saalmann and Kastner, 2015; Bourgeois et al, 2020; Kagan et al, 2021). Studies in human patients with unilateral thalamic lesions encompassing the pulvinar demonstrated deficits related to orienting or responding to perceptually or behaviorally salient stimuli in the contralesional hemifield (Danziger et al, 2001; Karnath et al, 2002; Arend et al, 2008b, 2008a; Lucas et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Dorsal pulvinar inactivation leads to spatial selection bias without perceptual deficit

Kaduk

Wilke

Kagan

2022

Preprint

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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.

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

Cited by 5 publications

References 143 publications

Cortico‐thalamocortical interactions for learning, memory and decision‐making

Cortico‐thalamocortical interactions for learning, memory and decision‐making

Visual, delay and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

Dorsal pulvinar inactivation leads to spatial selection bias without perceptual deficit

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