Control of adaptive action selection by secondary motor cortex during flexible visual categorization

Abstract

<jats:p>Adaptive action selection during stimulus categorization is an important feature of flexible behavior. To examine neural mechanism underlying this process, we trained mice to categorize the spatial frequencies of visual stimuli according to a boundary that changed between blocks of trials in a session. Using a model with a dynamic decision criterion, we found that sensory history was important for adaptive action selection after the switch of boundary. Bilateral inactivation of the secondary motor cortex (M2) impaired adaptive action selection by reducing the behavioral influence of sensory history. Electrophysiological recordings showed that M2 neurons carried more information about upcoming choice and previous sensory stimuli when sensorimotor association was being remapped than when it was stable. Thus, M2 causally contributes to flexible action selection during stimulus categorization, with the representations of upcoming choice and sensory history regulated by the demand to remap stimulus-action association.</jats:p>

A cortical circuit mechanism for structural knowledge-based flexible sensorimotor decision-making

“…For example, in a simple sensory stimulus categorization task, comparable accuracy of behavioral choices can be observed for well-learned stimuli or for newly encountered stimuli, with the former requiring only learned sensorimotor associations involving earlier sensorimotor areas but the latter requiring categorical decisions with generalization that involve higher association areas (Zhong et al, 2019). In the current study, although the behavioral expression of switching the categorization boundary is similar to that reported in other studies (Jaramillo et al, 2014;Wang et al, 2020), a crucial difference in task design determined the engagement of different underlying processes and neural mechanisms. The previous tasks used different sets of training stimuli between the two boundary conditions so that the animals primarily used the changes in sensory information to make different choices for the reversing stimuli between different conditions (Wang et al, 2020).…”

“…The occurrence of different sound stimuli was close in left or right trials (STAR Methods). This trial design, while maintaining balanced choice values, ensured that the primary information indicating the boundary change was from the choice outcomes in reversing trials instead of from large differences in stimulus compositions in different blocks, as in previously reported tasks (Jaramillo et al, 2014;Wang et al, 2020).…”

“…The auditory cortex has been shown to encode important perceptual decision information during stimulus categorization (Bizley and Cohen, 2013;Tsunada et al, 2016;Xin et al, 2019). The OFC has been implicated widely in flexible behavior (Schoenbaum et al, 2009;Wallis, 2007) and has been shown to project directly to sensory cortices (Zingg et al, 2014) to regulate sensory processing and sensorimotor associations (Banerjee et al, 2020;Liu et al, 2020;Winkowski et al, 2018). Here, using in vivo two-photon imaging from the auditory cortex, we found that a subpopulation of auditory cortex (ACx) neurons encode the category boundary estimate, a hidden variable associated with task structural knowledge.…”

Dynamics of history-dependent perceptual judgment

“…Consistent with this supposition, the prior can be manipulated separately from the short term buffer 44 . The short term buffer is not purposefully engaged in the present reference memory task; nevertheless, it plays a role by attracting μ (see also 55 ).…”

Activity in developing prefrontal cortex is shaped by sleep and sensory experience

“…That sleep so profoundly modulates neural activity in developing M1 raises the possibility that it also modulates higher-order prefrontal cortical areas with which M1 forms reciprocal connections, such as secondary motor cortex (M2) and medial prefrontal cortex (mPFC) (van Eden et al, 1992; Bedwell et al, 2014). As its name implies, M2 has a particularly close functional and anatomical connection with M1, integrating multimodal sensory cues for motor planning and modulating M1 activity during goal-directed action (Yin, 2009; Sul et al 2011; Omlor, 2016; Barthas and Kwan, 2017; Morandell and Huber, 2017; Wang et al, 2020). Like M1, M2 develops a somatotopic map, further highlighting its dependence on sensory input (Yin, 2009; Kunori and Takashima, 2016; Omlor, 2016; Barthas and Kwan, 2017; Chen et al, 2017; Singleton et al, 2021).…”