A distributed circuit for associating environmental context with motor choice in retrosplenial cortex

During navigation, animals often use recognition of familiar environmental contexts to guide motor action selection. The retrosplenial cortex (RSC) receives inputs from both visual cortex and subcortical regions required for spatial memory and projects to motor planning regions. However, it is not known whether RSC is important for associating familiar environmental contexts with specific motor actions. We test this possibility by developing a task in which motor trajectories are chosen based on the context. We find that mice exhibit differential predecision activity in RSC and that optogenetic suppression of RSC activity impairs task performance. Individual RSC neurons encode a range of task variables, often multiplexed with distinct temporal profiles. However, the responses are spatiotemporally organized, with task variables represented along a posterior-to-anterior gradient along RSC during the behavioral performance, consistent with histological characterization. These results reveal an anatomically organized retrosplenial cortical circuit for associating environmental contexts with appropriate motor outputs.

A Distributed Circuit for Associating Environmental Context to Motor Choice in Retrosplenial Cortex

ABSTRACTDuring navigation, animals often use recognition of familiar environmental contexts to guide motor action selection. The retrosplenial cortex (RSC) receives inputs from both visual cortex and subcortical regions required for spatial memory, and projects to motor planning regions. However, it is not known whether RSC is important for associating familiar environmental contexts with specific motor actions. Here, we test this possibility by developing a task in which trajectories are chosen based on the context. We find that mice exhibit differential pre-decision activity in RSC, and that optogenetic suppression of RSC activity impairs task performance. Individual RSC neurons encode a range of task variables, often multiplexed with distinct temporal profiles. However, the responses are spatiotemporally organized, with task variables represented along a posterior-to-anterior gradient along RSC during the behavioral performance, consistent with histological characterization. These results reveal an anatomically-organized retrosplenial cortical circuit for associating environmental contexts to appropriate motor outputs.

A Geometric Characterization of Population Coding in the Prefrontal Cortex and Hippocampus during a Paired-Associate Learning Task

Large-scale neuronal recording techniques have enabled discoveries of population-level mechanisms for neural computation. However, it is not clear how these mechanisms form by trial-and-error learning. In this article, we present an initial effort to characterize the population activity in monkey prefrontal cortex (PFC) and hippocampus (HPC) during the learning phase of a paired-associate task. To analyze the population data, we introduce the normalized distance, a dimensionless metric that describes the encoding of cognitive variables from the geometrical relationship among neural trajectories in state space. It is found that PFC exhibits a more sustained encoding of the visual stimuli, whereas HPC only transiently encodes the identity of the associate stimuli. Surprisingly, after learning, the neural activity is not reorganized to reflect the task structure, raising the possibility that learning is accompanied by some “silent” mechanism that does not explicitly change the neural representations. We did find partial evidence on the learning-dependent changes for some of the task variables. This study shows the feasibility of using normalized distance as a metric to characterize and compare population-level encoding of task variables and suggests further directions to explore learning-dependent changes in the neural circuits.

A functional hierarchy for choice in medial prefrontal cortex

SUMMARYHierarchical approaches to functional neuroanatomy propose that choice-relevant brain regions have overlapping functions and can be organized into a series that progressively transforms information about options into choices. Here, we examined responses of neurons in four regions of the medial prefrontal cortex as macaques performed two-option risky choices. All four regions encoded economic variables in similar proportions and showed putative signatures of key choice-related computations. We found evidence for a hierarchical organization proceeding from areas 14→25→32→24. Specifically, we found that decodability of eight distinct task variables increased along that path, consistent with the idea that hierarchically later regions make these variables more separable. We also found longer intrinsic timescales in the same series, further supporting the idea of a hierarchy. Together these results highlight the importance of the medial wall in choice, endorse a specific hierarchical organization, and argue against a modular functional neuroanatomy of choice.

Coordination amongst quadriceps muscles suggests neural regulation of internal joint stresses, not simplification of task performance

Many studies have demonstrated covariation between muscle activations during behavior, suggesting that muscles are not controlled independently. According to one common proposal, this covariation reflects simplification of task performance by the nervous system so that muscles with similar contributions to task variables are controlled together. Alternatively, this covariation might reflect regulation of low-level aspects of movements that are common across tasks, such as stresses within joints. We examined these issues by analyzing covariation patterns in quadriceps muscle activity during locomotion in rats. The three monoarticular quadriceps muscles (vastus medialis [VM], vastus lateralis [VL], and vastus intermedius [VI]) produce knee extension and so have identical contributions to task performance; the biarticular rectus femoris (RF) produces an additional hip flexion. Consistent with the proposal that muscle covariation is related to similarity of muscle actions on task variables, we found that the covariation between VM and VL was stronger than their covariations with RF. However, covariation between VM and VL was also stronger than their covariations with VI. Since all vastii have identical actions on task variables, this finding suggests that covariation between muscle activity is not solely driven by simplification of overt task performance. Instead, the preferentially strong covariation between VM and VL is consistent with the control of internal joint stresses: Since VM and VL produce opposing mediolateral forces on the patella, the high positive correlation between their activation minimizes the net mediolateral patellar force. These results provide important insights into the interpretation of muscle covariations and their role in movement control.

Identifying control structure of multi-joint coordination in dart throwing: the effect of distance constraint

Background: This study used the uncontrolled manifold (UCM) approach to study joint coordination underlying the control of task-related variables important for success at dart throwing skill. Success at a task can be achieved, in principle, by always adopting a particular joint combination. In contrast, we adopt a more selective control strategy: variations of the joint configuration that leave the values of essential task variables unchanged are predicted to be less controlled (i.e., stabilized to a lesser degree) than joint configuration changes that shift the values of the task variables. Objectives: How this abundance of motor solutions is managed by the nervous system and whether and how the throwing in different distances affects the solution to joint coordination was investigated in this study. Methods: Our experimental task involved dart throwing to a target under three conditions (standard, short and long distance) that it performed by fifteen dart professional and semiprofessional athletes. The four joint angles of the arm were obtained from the recorded positions of markers on the limb segments. The variability of joint configurations was decomposed into components lying parallel to those sets and components lying in their complement with respect to control of the path of the arm’s center of mass and spatial position of the hand. Results: When performing the task in all three different conditions, fluctuations of joint configuration that affected arm’s center of mass and spatial position variables were much reduced compared with fluctuations that did not affect these variables. The UCM principle applied to arm’s center of mass and spatial position thus captures the structure of the motor control system across different parts of joint configuration space as the movement evolves in time. Moreover, constraints representing an invariant arm’s center of mass or the spatial position structured joint configuration variability in the early and mid-portion of the movement trajectory, but not at the time of throwing. This specific control strategy indicate a target can be hit successfully also by controlling irrelevant directions in joint space equally to relevant ones. Conclusion: The results suggests a specific control strategy in which changes of joint configuration that are irrelevant to success at the task are selectively released from control. As a result, the method can be successfully used to determine the structure of coordination in joint space that underlies the control of the essential variables for a given task.

Coordination amongst quadriceps muscles suggests neural regulation of internal joint stresses, not simplification of task performance

SummaryMany studies have demonstrated co-variation between muscle activations during behavior, suggesting that muscles are not controlled independently. According to one common proposal, this co-variation reflects simplification of task performance by the nervous system, so that muscles with similar contributions to task variables are controlled together. Alternatively, this co-variation might reflect regulation of low-level aspects of movements that are common across tasks, such as stresses within joints. We examined these issues by analyzing co-variation patterns in quadriceps muscle activity during locomotion in rats. The three mono-articular quadriceps muscles (vastus medialis, VM; vastus lateralis, VL; vastus intermedius, VI) produce knee extension and so have identical contributions to task performance; the bi-articular rectus femoris (RF) produces an additional hip flexion. Consistent with the proposal that muscle co-variation is related to similarity of muscle actions on task variables, we found that the co-variation between VM and VL was stronger than their co-variations with RF. However, co-variation between VM and VL was also stronger than their co-variations with VI. Since all vastii have identical actions on task variables, this finding suggests that co-variation between muscle activity is not solely driven by simplification of task performance. Instead, the preferentially strong co-variation between VM and VL is consistent with the control of internal joint stresses: since VM and VL produce opposing mediolateral forces on the patella, the high positive correlation between their activation minimizes the net mediolateral patellar force. These results provide important insights into the interpretation of muscle co-variations and their role in movement control.