Thalamic control of functional cortical connectivity

Nakajima, Miho; Halassa, Michael M.

doi:10.1016/j.conb.2017.04.001

Cited by 161 publications

(112 citation statements)

References 42 publications

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“…The on-switch occurs et al, 2019). Furthermore, the dynamical entrainment of thalamus with cortex predicts tuning of thalamic neu-709 rons to task variables, consistent with a growing body 710 of work showing specificity in thalamic responses (Naka-711 jima andHalassa, 2017;Guo et al, 2017;Rikhye et al, motor thalamus should be tuned to movement properties, for much the same reasons that cortical neurons For this, they proposed a generic prepara-754 tory loop similar to the one we have studied here. How-755 ever, theirs does not take into account the degenera-756 cies in preparatory states induced by prospective mo-757 tor costs, which ours exploits.…”

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confidence: 76%

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Optimal anticipatory control as a theory of motor preparation: a thalamo-cortical circuit model

Kao

Sadabadi

Hennequin

2020

Preprint

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Across a range of motor and cognitive tasks, cortical activity can be accurately described by low-dimensional dynamics unfolding from specific initial conditions on every trial. These "preparatory states" largely determine the subsequent evolution of both neural activity and behaviour, and their importance raises questions regarding how they are -or ought to be -set. Here, we formulate motor preparation as optimal prospective control of future movements. The solution is a form of internal control of cortical circuit dynamics, which can be implemented as a thalamo-cortical loop gated by the basal ganglia. Critically, optimal control predicts selective quenching of variability in components of preparatory population activity that have future motor consequences, but not in others. This is consistent with recent perturbation experiments performed in mice, and with our novel analysis of monkey motor cortex activity during reaching. Together, these results suggest optimal anticipatory control of movement.Fast ballistic movements (e.g. throwing) require spa-1 lamocortical loop during motor preparation, with tha-62 lamic afferents providing the desired optimal control in-63 puts. This is consistent with the causal role of thalamus 64 in the preparation of directed licking in mice (Guo et al., 65 2017). Moreover, we posit that the basal ganglia oper-66 ate an on/off switch on the thalamocortical loop (Jin 67 and Costa, 2010; Cui et al., 2013; Halassa and Acsády, 68 2016; Logiaco et al., 2019), thereby flexibly controlling 69 the timing of both movement planning and initiation.70We further analyze the model, and formulate predic-71 tions which we have successfully tested in data. At the 72 most abstract level, our core prediction is that the "op-73 timal subspace" is likely high dimensional, with many 74 different initial conditions giving rise to the same cor-75 rect movement. This has an important consequence for 76 preparatory control: at the population level, only a few 77 components of preparatory activity impact future mo-78 tor outputs, and it is these components only that need 79 active controlling. In contrast, one expects substantial 80 pre-movement variability in other, inconsequential com-81 ponents. Concretely, we predict that following a pertur-82 bation, preparatory activity should recover only in state 83 space directions that matter for subsequent movement, 84 but not (necessarily) in others. We find that this pre-85 diction agrees with the effects of optogenetic perturba-86 tions reported by Svoboda and colleagues, in a directed 87 licking task in mice (Li et al., 2016). Furthermore, the 88 existence of a preparatory nullspace predicts selective 89 variability quenching at preparation onset: trial-by-trial 90 variability should drop predominantly in components 91 that have motor consequences. We perform novel analy-92 ses of monkey M1 and dorsal premotor cortex (PMd) ac-93 tivity recorded during reaching, and find that the struc-94 ture of variability quenching supports our main predic-95 tion. Finally...

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supporting

confidence: 76%

“…319mus acts as a relay station for cortical feedback(Guo 320 et al, 2017;Nakajima and Halassa, 2017). The loop 321 is gated on/off at preparation onset/offset by the 322 (dis)-inhibitory action of basal ganglia outputs(Jin and 323 Costa, 2010;Cui et al, 2013;Halassa and Acsády, 2016; 324 Logiaco et al, 2019).…”

mentioning

confidence: 99%

Optimal anticipatory control as a theory of motor preparation: a thalamo-cortical circuit model

Kao

Sadabadi

Hennequin

2020

Preprint

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“…The "cognitive thalamus" hypothesis postulates that the region is a key modulating hub for corticocortical interactions. [118][119][120] According to the hypothesis, high-order thalamic nuclei (ie, associative and posterior nuclei) exhibit critical functional and structural connections with the DMN, 71 thereby affecting network activity and, ultimately, cognition. The activity of high-order thalamic nuclei is under the control of cholinergic neurons that project from the PPN to the TRN.…”

Section: Thalamocortical Dysrhythmia As the Driver Of Dmn Decouplingmentioning

confidence: 99%

Hallucinations, somatic‐functional disorders of PD‐DLB as expressions of thalamic dysfunction

et al. 2019

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Hallucinations, delusions, and functional neurological manifestations (conversion and somatic symptom disorders) of Parkinson's disease (PD) and dementia with Lewy bodies increase in frequency with disease progression, predict the onset of cognitive decline, and eventually blend with and are concealed by dementia. These symptoms share the absence of reality constraints and can be considered comparable elements of the PD‐dementia with Lewy bodies psychosis. We propose that PD‐dementia with Lewy bodies psychotic disorders depend on thalamic dysfunction promoting a theta burst mode and subsequent thalamocortical dysrhythmia with focal cortical coherence to theta electroencephalogram rhythms. This theta electroencephalogram activity, also called fast‐theta or pre‐alpha, has been shown to predict cognitive decline and fluctuations in Parkinson's disease with dementia and dementia with Lewy bodies. These electroencephalogram alterations are now considered a predictive marker for progression to dementia. The resulting thalamocortical dysrhythmia inhibits the frontal attentional network and favors the decoupling of the default mode network. As the default mode network is involved in integration of self‐referential information into conscious perception, unconstrained default mode network activity, as revealed by recent imaging studies, leads to random formation of connections that link strong autobiographical correlates to trivial stimuli, thereby producing hallucinations, delusions, and functional neurological disorders. The thalamocortical dysrhythmia default mode network decoupling hypothesis provides the rationale for the design and testing of novel therapeutic pharmacological and nonpharmacological interventions in the context of PD, PD with dementia, and dementia with Lewy bodies. © 2019 International Parkinson and Movement Disorder Society

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“…Rather, patients managed distractions during encoding by amplifying the long‐range connectivity of other prefrontal DAN hubs (BA 8, 6) that modulate visuospatial WM (Christophel et al, ; du Boisgueheneuc et al, ; Kastner et al, ). Right superior frontal cortex (BA 8) connectivity was abnormally strengthened with the basal‐ganglia, thalamic nuclei that support spatial WM (dorsomedial and pulvinar) (Funahashi, ; Nakajima & Halassa, ), an encoding and recollection system (precuneus, posterior cingulate, PHC) (Cavanna & Trimble, ; Ranganath & Ritchey, ), and the ventral object processing system (middle and superior temporal) (Vilberg & Rugg, ). Left middle frontal (BA 6) connectivity was abnormally strengthened with the right inferior parietal cortex, an association area that subserves spatial functions (Singh‐Curry & Husain, ).…”

Section: Discussionmentioning

confidence: 99%

“…The PD group also failed to increase thalamus‐prefrontal connectivity (DLPFC, BA 10) when the burden on WM was greater, unlike the control group. The mediodorsal thalamus directs arousal in a context‐specific manner by amplifying local prefrontal cortex connectivity (Nakajima & Halassa, ; Schmitt et al, ), which serves to maintain representations active over time. PD patients who resembled control participants with respect to amplified load‐dependent mediodorsal thalamus connectivity also exhibited higher capacity and better distractor resistance.…”

Section: Discussionmentioning

confidence: 99%

Abnormal distraction and load‐specific connectivity during working memory in cognitively normal Parkinson's disease

Harrington

Shen

Filoteo

et al. 2019

Human Brain Mapping

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Visuospatial working memory impairments are common in Parkinson's disease (PD), yet the underlying neural mechanisms are poorly understood. The present study investigated abnormalities in context‐dependent functional connectivity of working memory hubs in PD. Cognitively normal PD and control participants underwent fMRI while performing a visuospatial working memory task. To identify sources of dysfunction, distraction, and load‐modulated connectivity were disentangled for encoding and retrieval phases of the task. Despite normal working memory performance in PD, two features of abnormal connectivity were observed, one due to a loss in normal context‐related connectivity and another related to upregulated connectivity of hubs for which the controls did not exhibit context‐dependent connectivity. During encoding, striatal‐prefrontal coupling was lost in PD, both during distraction and high memory loads. However, long‐range connectivity of prefrontal, medial temporal and occipital hubs was upregulated in a context‐specific manner. Memory retrieval was characterized by different aberrant connectivity patterns, wherein precuneus connectivity was upregulated during distraction, whereas prefrontal couplings were lost as memory load approached capacity limits. Features of abnormal functional connectivity in PD had pathological and compensatory influences as they correlated with poorer working memory or better visuospatial skills. The results offer new insights into working memory‐related signatures of aberrant cortico–cortical and corticostriatal functional connections, which may portend future declines in different facets of working memory.

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Thalamic control of functional cortical connectivity

Cited by 161 publications

References 42 publications

Optimal anticipatory control as a theory of motor preparation: a thalamo-cortical circuit model

Optimal anticipatory control as a theory of motor preparation: a thalamo-cortical circuit model

Hallucinations, somatic‐functional disorders of PD‐DLB as expressions of thalamic dysfunction

Abnormal distraction and load‐specific connectivity during working memory in cognitively normal Parkinson's disease

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