Sensory processing in humans and mice fluctuates between external and internal modes

Abstract

Perception is known to cycle through periods of enhanced and reduced sensitivity to external information. Here, we asked whether such slow fluctuations arise as a noise-related epiphenomenon of limited processing capacity or, alternatively, represent a structured mechanism of perceptual inference. Using 2 large-scale datasets, we found that humans and mice alternate between externally and internally oriented modes of sensory analysis. During external mode, perception aligns more closely with the external sensory information, whereas internal mode is characterized by enhanced biases toward perceptual history. Computational modeling indicated that dynamic changes in mode are enabled by 2 interlinked factors: (i) the integration of subsequent inputs over time and (ii) slow antiphase oscillations in the impact of external sensory information versus internal predictions that are provided by perceptual history. We propose that between-mode fluctuations generate unambiguous error signals that enable optimal inference in volatile environments.

N-Methyl-D-aspartate receptor hypofunction causes recurrent and transient failures of perceptual inference

“…Consistent with recent findings in humans and mice 16,17 , Bayesian model comparison indicated a clear superiority of the two-state GLM-HMM over the standard one-state GLM in the S-ketamine experiment (δ BIC = −3.65 × 10 3 ). According to the two-state GLM-HMM, perception fluctuated between an internal mode, shaped by the stabilizing internal prediction y t−1 , and an external mode, dominated by the SAR-weighted input s t .…”

“…We could not attribute between-mode transitions to fatigue, task difficulty (Figure 2D To our knowledge, these results are the first to uncover a neural mechanisms for the slow, task-related fluctuations in perceptual inference that have been observed across variety of tasks in humans and mice [14][15][16][17] . We found that healthy individuals who receive the NMDAR antagonist S-ketamine and patients diagnosed with Scz are prone to an external mode of perception.…”

“…fluctuations over time that occur at a timescale compatible with the duration of individual psychotic experiences [14][15][16] . Such fluctuations have been related to two opposing modes of inference, during which perception is driven predominantly either by external inputs or by internal predictions that stem from recent perceptual experiences 17 (Figure 1A). Although preliminary evidence indicates a tendency toward the external mode in people with Scz 18 , the neural mechanisms of mode fluctuations and their potential implications in psychosis have remained elusive.…”

Strategic stabilization of arousal boosts sustained attention

“…State-dependence of neural activity has been observed in primary sensory cortices (Goris et al, 2014;McGinley, David, et al, 2015;Musall et al, 2019;Nestvogel & McCormick, 2022) and sensory-guided behavior (McGinley, David, et al, 2015). More recently, spontaneous shifts between engaged, biased, and/or disengaged states have been inferred from behavior (Ashwood et al, 2022;Hulsey et al, 2023;Weilnhammer et al, 2023). However, the underlying causes and behavioral functions of these non-stationarities are not unclear.…”

Shifting attention between perception and working memory

“…Early behavioural studies used listreproduction tasks requiring verbal or manual reports of digits or letter series which were either perceptually available, stored in memory, or required integration across both domains (Carlson, Wenger, & Sullivan, 1993;Dark, 1990;Weber, Burt, & Noll, 1986). After a relative hiatus, the question of shifting attention between sensory and internally generated information has attracted renewed interest (Calzolari, Boneva, & Fernández-Espejo, 2022;Gilbert, Frith, & Burgess, 2005;Hautekiet, Verschooren, Langerock, & Vergauwe, 2023;Honey, Newman, & Schapiro, 2017;Poskanzer & Aly, 2023;Servais, Hurter, & Barbeau, 2023;Steel, Silson, Garcia, & Robertson, 2024;Treder et al, 2021;Verschooren, Liefooghe, Brass, & Pourtois, 2019;Verschooren, Pourtois, & Egner, 2020;Verschooren, Schindler, De Raedt, & Pourtois, 2019;Verschooren, Schindler, De Raedt, & Pourtois, 2021;Weilnhammer, Stuke, Standvoss, & Sterzer, 2023). For instance, researchers have replicated earlier work within the visual domain using tasks that require participants to shift between perception and memory on a trial-by-trial basis (Hautekiet et al, 2023;Verschooren et al, 2020;Verschooren, Liefooghe, et al, 2019).…”