Cognitive experience alters cortical involvement in navigation decisions

Abstract

The neural correlates of decision-making have been investigated extensively, and recent work aims to identify under what conditions cortex is actually necessary for making accurate decisions. We discovered that mice with distinct cognitive experiences, beyond sensory and motor learning, use different cortical areas and neural activity patterns to solve the same task, revealing past learning as a critical determinant of whether cortex is necessary for decision-making. We used optogenetics and calcium imaging to study the necessity and neural activity of multiple cortical areas in mice with different training histories. Posterior parietal cortex and retrosplenial cortex were mostly dispensable for accurate decision-making in mice performing a simple navigation-based decision task. In contrast, these areas were essential for the same simple task when mice were previously trained on complex tasks with delay periods or association switches. Multi-area calcium imaging showed that, in mice with complex-task experience, single-neuron activity had higher selectivity and neuron-neuron correlations were weaker, leading to codes with higher task information. Therefore, past experience sets the landscape for how future tasks are solved by the brain and is a key factor in determining whether cortical areas have a causal role in decision-making.

Shared and specialized coding across posterior cortical areas for dynamic navigation decisions

“…This hypothesis has similarities to theories that the cortex performs unsupervised learning on its inputs (Doya, 1999) and the machine learning concept of representation learning (Xie et al, 2020). In addition, results from the inactivation of the PPC and RSC in this and pre-vious studies are consistent with the notion that downstream areas use the posterior cortex's state representation to guide navigation decisions, instead of the PPC and RSC having a direct role in sensory perception or motor control, as inhibiting these areas eliminates associations between cue and choice without disrupting the mouse's ability to locomote or to perceive and respond to visual stimuli (Arlt et al, 2021;Harvey et al, 2012;Pinto et al, 2019). Furthermore, across studies, the PPC and RSC have been shown to be necessary for a variety of decision tasks that lack common computational requirements (Akrami et al, 2018;Arlt et al, 2021;Hwang et al, 2017;Lyamzin and Benucci, 2019), consistent with these areas participating in a general-purpose state representation.…”

“…Data from six out of seven mice for the photoinhibition experiments were included and analyzed differently as part of an independent study (Arlt et al, 2021). We started the photoinhibition after mice reached steady state performance within a rule block.…”

Functional (ir)Relevance of Posterior Parietal Cortex during Audiovisual Change Detection

“…Considering the broader literature on rodent PPC, under which task conditions would parietal circuitry be causally involved? In recent studies, stimuli and context were fixed while task demands were varied, and PPC, among other regions, became necessary only when evidence accumulation, working memory, or in any case an extension in the time scale of the task were required (Harvey et al, 2012;Pinto et al, 2019;Arlt et al, 2021). Our results fit with this view and suggest that PPC is dispensable for tasks that have fixed one-to-one sensorimotor mappings (but see Arlt et al, 2021).…”

“…In recent studies, stimuli and context were fixed while task demands were varied, and PPC, among other regions, became necessary only when evidence accumulation, working memory, or in any case an extension in the time scale of the task were required (Harvey et al, 2012;Pinto et al, 2019;Arlt et al, 2021). Our results fit with this view and suggest that PPC is dispensable for tasks that have fixed one-to-one sensorimotor mappings (but see Arlt et al, 2021). Along these lines, PPC is thought to participate in a larger cortical network constructing contextual representations of multimodal inputs.…”

How ‘visual’ is the visual cortex? The interactions between the visual cortex and other sensory, motivational and motor systems as enabling factors for visual perception

“…These areas, similarly to V1, are retinotopically organized [19,20] and play a significant role in processing visual information [21][22][23]. However, they have also long been shown to process other sensory modalities [24][25][26][27][28] and be involved in, for example, short-term memory, evidence accumulation and decision making [29][30][31][32][33]. For this reason, § §2 and 3 of this review will focus on V1, an area that, in contrast, is classically considered to be uniquely dedicated to visual processing.…”