A thalamocortical circuit encoding deviations from sensory history.
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| Title: | A thalamocortical circuit encoding deviations from sensory history. |
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| Authors: | Leow, Yi Ning (AUTHOR), Natesan, Arundhati (AUTHOR), Barlowe, Alexandria (AUTHOR), Ährlund-Richter, Sofie (AUTHOR), Luo, Tianyu (AUTHOR), Jazayeri, Mehrdad (AUTHOR), Sur, Mriganka (AUTHOR) |
| Source: | Science. 8/13/2026, Vol. 393 Issue 6812, p1-15. 15p. |
| Subjects: | Thalamocortical system, Decision making, Visual discrimination, Fluorescence microscopy, Thalamic nuclei, Optogenetics, Cingulate cortex, Sensory memory |
| Abstract: | Prior expectations guide attention and support perceptual filtering during decision-making. In mice performing a visual discrimination task, choices depended on trial-by-trial differences between consecutive stimuli (|ΔDir|). We hypothesized that thalamic lateral posterior (LP; rodent pulvinar) projections to prefrontal areas such as the anterior cingulate cortex (ACC), previously implicated in selective attention and predictive processing, could support history-dependent evaluation of current sensory evidence. In this work, we report that optogenetic manipulations of LP-ACC axons disrupted history-dependent evaluation of current sensory evidence, producing |ΔDir|-dependent choice biases. Two-photon imaging showed that LP-ACC axons represented stimuli along a task-dependent low-dimensional curved manifold whose geometry scaled with |ΔDir|, emphasizing larger deviations from recent evidence. These findings identify the LP-ACC as a thalamocortical pathway that implements a contrastive, history-referenced representation of sensory evidence during decisions. Editor's summary: Past experiences guide future decisions. Leow et al. studied the brain circuits mediating experience-dependent decision-making in mice. Using a combination of behavioral testing, optogenetic manipulation, calcium imaging, and computational techniques, the study reports that the thalamic lateral posterior nucleus–to–anterior cingulate cortex (LP-ACC) pathway uses information from the previous trial to guide adaptive decision-making. Manipulating LP-ACC disrupted the ability to use prior experiences to guide decisions. Further, calcium-imaging experiments showed that LP-ACC axons represent stimuli in a low-dimensional space, with each stimulus expressed as a point on a curved manifold encoding both stimulus direction and difficulty. This study highlights the key role of the thalamus in high-level cognition. —Mattia Maroso INTRODUCTION: Prior experience can powerfully shape ongoing perception and behavior. But how recent experience alters the brain's processing of ongoing sensory input remains unclear. The higher-order thalamic lateral posterior nucleus (LP; rodent pulvinar) is known to contribute to selective visual processing, whereas the anterior cingulate cortex (ACC) is implicated in evaluating evidence and guiding action, which makes the LP-ACC pathway a compelling candidate for linking recent experience to ongoing decisions. RATIONALE: We trained mice on a random dot motion discrimination task, which allowed us to quantify the trial-to-trial difference between current and previous motion evidence (∣ΔDir∣) and test how ongoing stimulus input is evaluated relative to recent sensory history. Optogenetic stimulation was performed to address whether perturbing LP-ACC input was sufficient to bias how evidence is converted into choice as a function of |∆Dir|. We then used two-photon imaging of LP-ACC axons to examine the structure of the information conveyed by this pathway, investigating whether recent sensory history reshapes the population representation of current motion evidence. These approaches enabled us to test specific computational roles for the LP-ACC pathway in comparing current and recent sensory evidence and to formulate a theoretical framework linking this computation to how current evidence is weighted and when choices are updated. RESULTS: Mice performed the task with their choices varying with trial-to-trial differences in motion evidence (∣ΔDir∣), indicating graded comparison across successive stimuli rather than a simple serial choice bias. Optogenetic activation of LP-ACC axons unilaterally biased choices toward the stimulated side in a manner that scaled with |∆Dir|, which shows that this pathway influences graded history-dependent evaluation of current sensory evidence rather than inducing a motor choice bias. Two-photon imaging revealed that LP-ACC axons transform current visual evidence into a task-gated low-dimensional population representation, with stimulus evidence organized along a curved trajectory. This representation jointly encoded stimulus direction and coherence and expanded with greater |∆Dir|, increasing the separation between stimuli when current evidence deviated more strongly from recent history. This provided evidence that LP-ACC axons encode current stimuli relative to recent sensory history. LP-ACC axons implemented a contrastive code across successive stimuli, such that peak responses were evoked when the current stimulus carried strong evidence for their preferred direction and was maximally different from the previous stimulus. Our imaging results further established that unlike ACC neurons, LP-ACC axons encoded information in a stimulus- rather than choice-centered reference frame. To understand how stimulus-anchored LP signals could lead to optogenetically induced choice biases, we developed a model with simulated perturbations to explain how LP-derived |∆Dir| signals to the ACC could influence the weighting of current evidence, probability of choice updating, and direction of choice. CONCLUSION: Our findings identify the LP-ACC as a thalamocortical pathway that implements a history-dependent contrastive computation, emphasizing deviations from recent sensory history to shape decision updating. More broadly, our results highlight how the higher-order thalamus can contribute to cognitive computation by embedding recent experience into ongoing sensory representations to guide behavior. The LP-ACC encodes current sensory evidence relative to recent history.: In a two-alternative choice random dot direction discrimination task, the LP provides the ACC with inputs that represent the difference in evidence between current and previous stimuli (∣ΔDir∣), emphasizing deviations through history-dependent expansion of a curved neural manifold representing current evidence. Greater |∆Dir| expands manifold representations and promotes updating. These inputs influence choice arbitration at the ACC, resulting in |∆Dir|-dependent psychometric behavior. StimL, left stimulus; StimR, right stimulus; P(ChooseR), probability of choosing right. [ABSTRACT FROM AUTHOR] |
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| Database: | Psychology and Behavioral Sciences Collection |
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