Expectation-induced modulation of metastable activity underlies faster coding of sensory stimuli

Abstract

1Sensory stimuli can be recognized more rapidly when they are expected. This 2 phenomenon depends on expectation affecting the cortical processing of sensory 3 information. However, virtually nothing is known on the mechanisms responsible for 4 the effects of expectation on sensory networks. Here, we report a novel computational 5 mechanism underlying the expectation-dependent acceleration of coding observed in 6 the gustatory cortex (GC) of alert rats. We use a recurrent spiking network model with a 7 clustered architecture capturing essential features of cortical activity, including the 8 metastable activity observed in GC before and after gustatory stimulation. Relying both 9 on network theory and computer simulations, we propose that expectation exerts its 10 function by modulating the intrinsically generated dynamics preceding taste delivery. 11Our model, whose predictions are confirmed in the experimental data, demonstrates 12 how the modulation of intrinsic metastable activity can shape sensory coding and 13 mediate cognitive processes such as the expectation of relevant events. Altogether, these 14 results provide a biologically plausible theory of expectation and ascribe a new 15 functional role to intrinsically generated, metastable activity. 16 17

Oxytocin differentially modulates amygdala responses during top-down and bottom-up aversive anticipation

“…Expected stimuli can be recognized more rapidly than unexpected ones (Mazzucato et al, 2019;Pinto et al, 2015;Samuelsen et al, 2012;Sussman et al, 2016a). Top-down modulation of visual processing involves visual cortical areas, which is involved with object recognition, as well as parietal and prefrontal cortex, which is involved with visually guided movements and attentional control (Gilbert and Li, 2013).…”

“…Relative to stimulus-driven bottom-up processes, top-down processes take into account cues or goals indicating upcoming threat-related stimuli. These anticipatory cues or goals may contribute to perceptual and attentional prioritization of threatening stimuli (Mazzucato et al, 2019;Yoshida and Katz, 2011). To determine the top-down and bottom-up mechanisms during the present emotion regulation task, we extracted the time courses from hub regions of the visual and visuospatial attention networks and observed that top-down anticipatory cues modulated the temporal dynamics of sensory coding and attention control.…”

“…Consequently dysregulations in the fine-grained interplay between the generation and regulation of negative emotions represent transdiagnostic deficits across major psychiatric disorders (Sloan et al, they may also contribute to perceptual and attentional prioritization of threatening stimuli such that anticipatory cues can accelerate stimulus coding in the visual and attention systems (Hahn and Gronlund, 2007;Mazzucato et al, 2019;Sussman et al, 2016a;Yoshida and Katz, 2011).…”

Metastable attractors explain the variable timing of stable behavioral action sequences

“…S7). One may drive clustered networks with strong time-dependent stimuli to pace activity along stimulus-specific sequences [12,21,25,26,68]. However, this would merely shift the problem of reliable sequence generation from the local circuit to an upstream area producing the specific input (but see [69]).…”

“…Previous work showed that the activity patterns, revealed by hidden Markov models, can be interpreted as metastable attractors, arising from recurrent dynamics in local cortical circuits [12,21]. Metastable attractors are produced in biologically plausible network models [22,23] and have been used to elucidate features of sensory processing [12,21], working memory [24] and expectation [25], and to explain state-dependent modulations of neural variability [22,23,26]. However, while previous models are capable of generating sequential activity [21,[27][28][29], they are hindered by a fundamental trade-off between sequence reproducibility and trial-to-trial temporal variability.…”