Context-Dependent Sensory Processing across Primary and Secondary Somatosensory Cortex

SUMMARY

To interpret the environment, our brain must evaluate external stimuli against internal representations from past experiences. How primary (S1) and secondary (S2) somatosensory cortices process stimuli depending on recent experiences is unclear. Using simultaneous multi-area population imaging of projection neurons and focal optogenetic inactivation,we studied mice performing a whisker-based working memory task. We find that activity reflecting a current stimulus, the recollection of a previous stimulus (cued recall), and the stimulus category are
distributed across S1 and S2. Despite this overlapping representation, S2 is important for processing cued recall responses and transmitting these responses to S1. S2 network properties differ from S1, wherein S2 persistently encodes cued recall and the stimulus category under passive conditions.
Although both areas encode the stimulus category, only information in S1 is important for task performance through pathways that do not necessarily include S2. These findings reveal both distributed and segregated roles for S1 and S2 in context-dependent sensory processing.

INTRODUCTION

How a sensory stimulus is interpreted depends on the context in which it is perceived. This context can include other incoming stimuli from the surrounding sensory scene or can be composed
of internal representations of relevant past sensory experiences and behavioral states (Khan and Hofer, 2018). Contextdependent sensory processing can produce new categorical representations that can reflect the integration and comparison of past and present stimuli (Miller et al., 1991; Romo et al., 2012).
How the neocortex is organized to produce such category representations is largely unclear. Sensory cortices are parcellated into primary and higher areas in which neurons in higher areas can encode for increasingly invariant representations (DiCarlo et al., 2012; Kitada, 2016). However, the extentto which context-dependent sensory processing occurs in a serial, hierarchical manner (Felleman and Van Essen, 1991) or in a distributed fashion (Rumelhart and McClelland, 1987; Siegel et al., 2015) across these cortical areas remains a topic of
debate.
The recent availability of increasingly large-scale, cellular recording techniques now enables a thorough survey of the diversity of neuronal responses and the dynamic interactions that exist across cortical areas (Jun et al., 2017; Sofroniew et al., 2016). New evidence suggests that the encoding of task-related information can be highly distributed across related cortical areas, which supports the notion of a distributed network for perceptual processing (Chen et al., 2016; Herna´ ndez et al., 2010; Koay et al., 2019; Minderer et al., 2019; Steinmetz et al., 2018). However, functional recordings alone do not provide insight as to whether such widespread signals are due to local processing within an area or the inheritance of information from other connected areas. Therefore, population coding and information flow between areas must also be tracked. Further, functional perturbations in each area must be performed to determine whether information
available locally within an area is necessary for sensory-driven behavior.
Here, we investigate how the primary (S1) and secondary (S2) whisker somatosensory cortex operate and interact to process tactile stimuli and their related context. Large-scale multi-area imaging across S1 and S2 confirms the presence of a distributed code in which both areas contain activity that reflects the present stimulus, the recall of recent stimulus representations, and stimulus context. However, through local optogenetic inactivation and activity measurements in anatomically identified corticocortical projection neurons, we find that the functional roles of these areas are not identical but instead reflect computations where the processing of recently recalled sensory stimuli can

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