skip to main content

Title: 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.
Authors:
;
Award ID(s):
1934288 1707287
Publication Date:
NSF-PAR ID:
10313317
Journal Name:
Science Advances
Volume:
7
Issue:
35
ISSN:
2375-2548
Sponsoring Org:
National Science Foundation
More Like this
  1. Environmental change can lead decision makers to shift rapidly among different behavioral regimes. These behavioral shifts can be accompanied by rapid changes in the firing pattern of neural networks. However, it is unknown what the populations of neurons that participate in such “network reset” phenomena are representing. Here, we investigated the following: (1) whether and where rapid changes in multivariate activity patterns are observable with fMRI during periods of rapid behavioral change and (2) what types of representations give rise to these phenomena. We did so by examining fluctuations in multivoxel patterns of BOLD activity from male and female human subjects making sequential inferences about the state of a partially observable and discontinuously changing variable. We found that, within the context of this sequential inference task, the multivariate patterns of activity in a number of cortical regions contain representations that change more rapidly during periods of uncertainty following a change in behavioral context. In motor cortex, this phenomenon was indicative of discontinuous change in behavioral outputs, whereas in visual regions, the same basic phenomenon was evoked by tracking of salient environmental changes. In most other cortical regions, including dorsolateral prefrontal and anterior cingulate cortex, the phenomenon was most consistent withmore »directly encoding the degree of uncertainty. However, in a few other regions, including orbitofrontal cortex, the phenomenon was best explained by representations of a shifting context that evolve more rapidly during periods of rapid learning. These representations may provide a dynamic substrate for learning that facilitates rapid disengagement from learned responses during periods of change.« less
  2. Abstract

    Rapid and flexible learning during behavioral choices is critical to our daily endeavors and constitutes a hallmark of dynamic reasoning. An important paradigm to examine flexible behavior involves learning new arbitrary associations mapping visual inputs to motor outputs. We conjectured that visuomotor rules are instantiated by translating visual signals into actions through dynamic interactions between visual, frontal and motor cortex. We evaluated the neural representation of such visuomotor rules by performing intracranial field potential recordings in epilepsy subjects during a rule-learning delayed match-to-behavior task. Learning new visuomotor mappings led to the emergence of specific responses associating visual signals with motor outputs in 3 anatomical clusters in frontal, anteroventral temporal and posterior parietal cortex. After learning, mapping selective signals during the delay period showed interactions with visual and motor signals. These observations provide initial steps towards elucidating the dynamic circuits underlying flexible behavior and how communication between subregions of frontal, temporal, and parietal cortex leads to rapid learning of task-relevant choices.

  3. Cortical representations expand during skilled motor learning. We studied a unique model of motor learning with cellular phone texting, where the thumbs are used exclusively to interact with the device and the prominence of use can be seen where 3200 text messages are exchanged a month in the 18–24 age demographic. The purpose of the present study was to examine the motor cortex representation and input–output (IO) recruitment curves of the abductor pollicis brevis (APB) muscle of the thumb and the ADM muscle with transcranial magnetic stimulation (TMS), relative to individuals’ texting abilities and short-term texting practice. Eighteen individuals performed a functional texting task (FTT) where we scored their texting speed and accuracy. TMS was then used to examine the cortical volumes and areas of activity in the two muscles and IO curves were constructed to measure excitability. Subjects also performed a 10-min practice texting task, after which we repeated the cortical measures. There were no associations between the cortical measures and the FTT scores before practice. However, after practice the APB cortical map expanded and excitability increased, whereas the ADM map constricted. The increase in the active cortical areas in APB correlated with the improvement in the FTT score.more »Based on the homogenous group of subjects that were already good at texting, we conclude that the cortical representations and excitability for the thumb muscle were already enlarged and more receptive to changes with short-term practice, as noted by the increase in FTT performance after 10-min of practice.« less
  4. Most sensorimotor studies investigating the covariation of populations of neurons in primary motor cortex (M1) have considered only a few trained movements made under highly constrained conditions. However, motor behaviors in daily living happen in a far more complex and varied contexts. It is unclear whether M1 neurons would have different population responses in a more naturalistic, unconstrained setting, including requirements to accommodate multiple limbs and body posture, and more extensive proprioceptive inputs. Here, we recorded M1 spiking signals while a monkey performed hand grasp movements in two different contexts: one in the typical constrained lab setting, and the other while moving freely in a large plastic cage. We compared the covariance patterns of the neural activity during movements across the two contexts. We found that the neural covariation patterns accompanying two different hand grasps in the unconstrained context were largely preserved, while they differed across contexts, even for the same type of grasp. We also found that the M1 population activity was confined to context-dependent neural manifolds, but these manifolds were not completely independent, as some dimensions appeared to be shared across the contexts. These results suggest that the coordinated activity of M1 neurons is strongly dependent on behavioralmore »context, in ways that were not entirely anticipated.« less
  5. Abstract

    The synaptic homeostasis theory of sleep proposes that low neurotransmitter activity in sleep optimizes memory consolidation. We tested this theory by asking whether increasing acetylcholine levels during early sleep would weaken motor memory consolidation. We trained separate groups of adult mice on the rotarod walking task and the single pellet reaching task, and after training, administered physostigmine, an acetylcholinesterase inhibitor, to increase cholinergic tone in subsequent sleep. Post-sleep testing showed that physostigmine impaired motor skill acquisition of both tasks. Home-cage video monitoring and electrophysiology revealed that physostigmine disrupted sleep structure, delayed non-rapid-eye-movement sleep onset, and reduced slow-wave power in the hippocampus and cortex. Additional experiments showed that: (1) the impaired performance associated with physostigmine was not due to its effects on sleep structure, as 1 h of sleep deprivation after training did not impair rotarod performance, (2) a reduction in cholinergic tone by inactivation of cholinergic neurons during early sleep did not affect rotarod performance, and (3) stimulating or blocking muscarinic and nicotinic acetylcholine receptors did not impair rotarod performance. Taken together, the experiments suggest that the increased slow wave activity and inactivation of both muscarinic and nicotinic receptors during early sleep due to reduced acetylcholine contribute to motormore »memory consolidation.

    « less