Action Selection and Flexible Switching Controlled by the Intralaminar Thalamic Neurons

Kato, Shigeki; Fukabori, Ryoji; Nishizawa, Kayo; Okada, Katsuhide; Yoshioka, Nozomu; Sugawara, Masateru; Maejima, Yuko; Shimomura, Kenju; Okamoto, Masahiro; Eifuku, Satoshi; Kobayashi, Kazuto

doi:10.1016/j.celrep.2018.02.016

Cited by 58 publications

(69 citation statements)

References 62 publications

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“…the parafascicular nucleus and the rostral intralaminar and midline nuclei 49,[51][52][53][54] . Because projections originating from different thalamic nuclei 25,52,163 and even from different subpopulations within these nuclei 49 , can have distinct properties and functions 51,52,59,60,164,165 , it remains to be seen which of these projections play a role in motor sequence execution, and whether they have distinct functions. Furthermore, while the totality of our results points to plasticity at thalamostriatal synapses as an important mechanism for motor learning, this too must be conclusively established.…”

Section: New Role For Thalamus In Learned Motor Sequence Executionmentioning

confidence: 99%

“…The thalamostriatal projection has been implicated in modulating activity of cortical inputs to striatum via cholinergic interneurons ( Fig. 1A), in the regulation of attention and behavioral flexibility, and in providing information to the BG about behavioral state and context for rapid behavioral adaptations [58][59][60][61][62][63][64] . Yet, whether they play a more direct role in motor learning and execution remains unclear.…”

Section: Introductionmentioning

confidence: 99%

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Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Wolff

Ölveczky

2019

Preprint

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The acquisition and execution of learned motor sequences are mediated by a distributed motor network, spanning cortical and subcortical brain areas. The sensorimotor striatum is an important cog in this network, yet how its two main inputs, from motor cortex and thalamus respectively, contribute to its role in motor learning and execution remains largely unknown. To address this, we trained rats in a task that produces highly stereotyped and idiosyncratic motor sequences. We found that motor cortical input to the sensorimotor striatum is critical for the learning process, but after the behaviors were consolidated, this corticostriatal pathway became dispensable. Functional silencing of striatal-projecting thalamic neurons, however, disrupted the execution of the learned motor sequences, causing rats to revert to behaviors produced early in learning and preventing them from re-learning the task. These results show that the sensorimotor striatum is a conduit through which motor cortical inputs can drive experiencedependent changes in subcortical motor circuits, likely at thalamostriatal synapses.

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Section: New Role For Thalamus In Learned Motor Sequence Executionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Wolff

Ölveczky

2019

Preprint

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“…The mediodorsal (MD) and rostral intralaminar (IL) thalamic nuclei interact with the prefrontal cortex (PFC) and striatum to promote flexible selection of adaptive actions (Halassa & Kastner, ; Kato et al., ; Parnaudeau, Bolkan, & Kellendonk, ; Varela, ). Rodent medial PFC (mPFC) receives substantial projections from limbic and non‐limbic cortices and other forebrain and brainstem areas that provide extensive information about external and internal environments, previous events, and planned and ongoing sensorimotor activity (Hoover & Vertes, ).…”

Section: Introductionmentioning

confidence: 99%

“…Early studies emphasized effects of MD and IL lesions on working memory in delayed conditional discriminations and described impairments appearing at memory delays from 1 to 30 s in different studies (Aggleton & Mishkin, ; Bailey & Mair, ; Isseroff, Rosvold, Galkin, & Goldman‐Rakic, ; Mair, Burk, & Porter, ; Young, Stevens, Kivlahan, & Mair, ; Zola‐Morgan & Squire, ). Other studies have revealed effects of MD and IL lesions on choices that do not require working memory (Kato et al., ; Newman & Burk, ; Parnaudeau et al., , ; Stevens & Mair, ; Wolff, Faugére, Desfosses, Coutureau, & Marchand, ) as well as the abilities to utilize action‐outcome associations and to learn instrumental actions (Bradfield, Hart, & Balleine, ; Corbit, Muir, & Balleine, ; Mitchell, ). These results suggest an important role for the central thalamus in reinforcement‐guided responding that extends beyond working memory.…”

Section: Introductionmentioning

confidence: 99%

Central thalamic inactivation impairs the expression of action‐ and outcome‐related responses of medial prefrontal cortex neurons in the rat

Francoeur

Wormwood

Gibson

et al. 2019

Eur J of Neuroscience

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The mediodorsal (MD) and adjacent intralaminar (IL) and midline nuclei provide the main thalamic input to the medial prefrontal cortex (mPFC) and are critical for associative learning and decision‐making. MD neurons exhibit activity related to actions and outcomes that mirror responses of mPFC neurons in rats during dynamic delayed non‐match to position (dDNMTP), a variation of DNMTP where start location is varied randomly within an open octagonal arena to avoid confounding behavioral events with spatial location. To test whether the thalamus affects the expression of these responses in mPFC, we inhibited the central thalamus unilaterally by microinjecting muscimol at doses and sites found to affect decision‐making when applied bilaterally. Unilateral inactivation reduced normalized task‐related responses in the ipsilateral mPFC without disrupting behavior needed to characterize event‐related neuronal activity. Our results extend earlier findings that focused on delay‐related activity by showing that central thalamic inactivation interferes with responses related to actions and outcomes that occur outside the period of memory delay. These findings are consistent with the broad effects of central thalamic lesions on behavioral measures of reinforcement‐guided responding. Most (7/8) of the prefrontal response types affected by thalamic inactivation have also been observed in MD during dDNMTP. These results support the hypothesis that MD and IL act as transthalamic gates: monitoring prefrontal activity through corticothalamic inputs; integrating this information with signals from motivational and sensorimotor systems that converge in thalamus; and acting through thalamocortical projections to enhance expression of neuronal responses in the PFC that support adaptive goal‐directed behavior.

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“…The critical contribution of PFC activity to set-shifting may be mediated by a number of output pathways, but two PFC projection targets of particular interest are the projection to ventromedial striatum (PFC-VMS) and to the medio-dorsal thalamus (PFC-MDT). In rodents, both target structures have established roles in set-shifting behavior [19][20][21][22] , and PFC projections to both structures underlie behavioral flexibility behavior 23,24 .…”

Section: Introductionmentioning

confidence: 99%

Prefrontal deep projection neurons enable cognitive flexibility via persistent feedback monitoring

Spellman

Svei

Liston

2019

Preprint

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Cognitive flexibility, the ability to alter one's strategy in light of changing stimulus-response-reward relationships, is a critical tool for acquiring and executing learned behavior. In order to adapt to novel, uncertain, or dynamic contexts, it is often necessary to abandon previously successful rules, and explore new rules, based on trial and error. One form of cognitive flexibility, commonly referred to as set-shifting, entails ignoring a previously relevant stimulus feature in favor of a newly relevant features. Successful performance of set-shifting behavior has been shown through previous work to involve the prefrontal cortex (PFC), and impairments in setshifting behavior are associated with multiple psychiatric disorders. In spite of the translational importance of this behavior, it remains unclear which cell types within PFC are responsible for conveying information critical to setshifting to downstream brain regions. To address this question, we used a novel set-shifting task in head-fixed mice to test the role of two major PFC projections, the cortico-striatal and cortico-thalamic pathways, in setshifting. Using optogenetics and 2-photon calcium imaging, we found that these cell types robustly and persistently encoded feedback from the outcomes of recent trials, and that the activity of both cell types during the inter-trial interval was critical to successfully switching between task rules. Moreover, we found that both cell types displayed a topological gradient, with neurons located further from the pial surface representing more taskcritical information. Together, these findings suggest that deep PFC projection neurons enable set-shifting through trial feedback monitoring. Figure 1 a) Task schematic. Top: diagram of stimulus delivery and lick response setup. Bottom: relevant and irrelevant stimuli and rule shifting. b) Training curves for seven learning stages. Y-axis denotes the proportion of animals at a given learning stage after trial number x. SD = Simple Discrimination, CD = Compound Discrimination, IDS1 = Intradimensional Shift (initial stimulus modality), Rev = Reversal (initial stimulus modality), EDS = Extradimensional Shift, IDS2 = Intradimensional Shift (second stimulus modality), SEDS = Serial Extradimensional Shifting. N = 53 animals. Trials displayed are concatenated from across multiple sessions (Mode = 350 trials/session). c) Left: Number of trials to criterion, Intradimensional vs Extradimensional Shift, n = 53 animals, sign rank = 0.0034, 6*10^-5 for IDS1/EDS, IDS2/EDS, 0.2for IDS1/IDS2. Right: Mean trials to criterion during SEDS, whisker rule vs odor rule. N = 100 animals, signed rank = 0.45. d) Left: trials to criterion in EDS sessions following transcranial infusion (SAL = saline; MUS = muscimol). N = 12, 13 (SAL, MUS). Rank sum p = 0.02.Right: Number of trial blocks reaching criterion performance in SEDS sessions following 10 rule shifts. N = 12; median blocks (BL/MUS/SAL): 4, 1.5, 4. Sign rank p = 0.0005 (BL/MUS), 0.001 (SAL/MUS), 0.68 (BL/SAL). Median total trials complete...

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Action Selection and Flexible Switching Controlled by the Intralaminar Thalamic Neurons

Cited by 58 publications

References 62 publications

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Central thalamic inactivation impairs the expression of action‐ and outcome‐related responses of medial prefrontal cortex neurons in the rat

Prefrontal deep projection neurons enable cognitive flexibility via persistent feedback monitoring

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