Distinct neural representations during a brain-machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum.

Although brain-machine interfaces (BMIs) are directly controlled by the modulation of a select local population of neurons, distributed networks consisting of cortical and subcortical areas have been implicated in learning and maintaining control. Previous work in rodents has demonstrated the involvement of the striatum in BMI learning. However, the prefrontal cortex has been largely ignored when studying motor BMI control despite its role in action planning, action selection, and learning abstract tasks. Here, we compare local field potentials simultaneously recorded from primary motor cortex (M1), dorsolateral prefrontal cortex (DLPFC), and the caudate nucleus of the striatum (Cd) while nonhuman primates perform a two-dimensional, self-initiated, center-out task under BMI control and manual control. Our results demonstrate the presence of distinct neural representations for BMI and manual control in M1, DLPFC, and Cd. We find that neural activity from DLPFC and M1 best distinguishes control types at the go cue and target acquisition, respectively, while M1 best predicts target-direction at both task events. We also find effective connectivity from DLPFC → M1 throughout both control types and Cd → M1 during BMI control. These results suggest distributed network activity between M1, DLPFC, and Cd during BMI control that is similar yet distinct from manual control.

Distinct neural representations during a brain-machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum.

Although brain-machine interfaces (BMIs) are directly controlled by the modulation of a select local population of neurons, distributed networks consisting of cortical and subcortical areas have been implicated in learning and maintaining control. Previous work in rodent BMI has demonstrated the involvement of the striatum in BMI learning. However, the prefrontal cortex has been largely ignored when studying motor BMI control despite its role in action planning, action selection, and learning abstract tasks. Here, we compare local field potentials simultaneously recorded from the primary motor cortex (M1), dorsolateral prefrontal cortex (DLPFC), and the caudate nucleus of the striatum (Cd) while nonhuman primates perform a two-dimensional, self-initiated, center-out task under BMI control and manual control. Our results demonstrate the presence of distinct neural representations for BMI and manual control in M1, DLPFC, and Cd. We find that neural activity from DLPFC and M1 best distinguish between control types at the go cue and target acquisition, respectively. We also found effective connectivity from DLPFC→M1 throughout trials across both control types and Cd→M1 during BMI control. These results suggest distributed network activity between M1, DLPFC, and Cd during BMI control that is similar yet distinct from manual control.

Memory reactivation and suppression modulate integration of the semantic features of related memories in hippocampus.

Encoding an event that overlaps with a previous experience may involve reactivating an existing memory and integrating it with new information or suppressing the existing memory to promote formation of a distinct, new representation. We used fMRI during overlapping event encoding to track reactivation and suppression of individual, related memories. We further used a model of semantic knowledge based on Wikipedia to quantify both reactivation of semantic knowledge related to a previous event and formation of integrated memories containing semantic features of both events. Representational similarity analysis revealed that reactivation of semantic knowledge related to a prior event in posterior medial prefrontal cortex (pmPFC) supported memory integration during new learning. Moreover, anterior hippocampus (aHPC) formed integrated representations combining the semantic features of overlapping events. We further found evidence that aHPC integration may be modulated on a trial-by-trial basis by interactions between ventrolateral PFC and anterior mPFC, with suppression of item-specific memory representations in anterior mPFC inhibiting hippocampal integration. These results suggest that PFC-mediated control processes determine the availability of specific relevant memories during new learning, thus impacting hippocampal memory integration.

Selective modulation of cortical population dynamics during neuroprosthetic skill learning.

Brain-machine interfaces (BMIs) provide a framework for studying how cortical population dynamics evolve over learning in a task in which the mapping between neural activity and behavior is precisely defined. Learning to control a BMI is associated with the emergence of coordinated neural dynamics in populations of neurons whose activity serves as direct input to the BMI decoder (direct subpopulation). While previous work shows differential modification of firing rate modulation in this population relative to a population whose activity was not directly input to the BMI decoder (indirect subpopulation), little is known about how learning-related changes in cortical population dynamics within these groups compare.To investigate this, we monitored both direct and indirect subpopulations as two macaque monkeys learned to control a BMI. We found that while the combined population increased coordinated neural dynamics, this increase in coordination was primarily driven by changes in the direct subpopulation. These findings suggest that motor cortex refines cortical dynamics by increasing neural variance throughout the entire population during learning, with a more pronounced coordination of firing activity in subpopulations that are causally linked to behavior.

Semantic Knowledge of Famous People and Places Is Represented in Hippocampus and Distinct Cortical Networks.

Studies have found that anterior temporal lobe (ATL) is critical for detailed knowledge of object categories, suggesting that it has an important role in semantic memory. However, in addition to information about entities, such as people and objects, semantic memory also encompasses information about places. We tested predictions stemming from the PMAT model, which proposes there are distinct systems that support different kinds of semantic knowledge: an anterior temporal (AT) network, which represents information about entities; and a posterior medial (PM) network, which represents information about places. We used representational similarity analysis to test for activation of semantic features when human participants viewed pictures of famous people and places, while controlling for visual similarity. We used machine learning techniques to quantify the semantic similarity of items based on encyclopedic knowledge in the Wikipedia page for each item and found that these similarity models accurately predict human similarity judgments. We found that regions within the AT network, including ATL and inferior frontal gyrus, represented detailed semantic knowledge of people. In contrast, semantic knowledge of places was represented within PM network areas, including precuneus, posterior cingulate cortex, angular gyrus, and parahippocampal cortex. Finally, we found that hippocampus, which has been proposed to serve as an interface between the AT and PM networks, represented fine-grained semantic similarity for both individual people and places. Our results provide evidence that semantic knowledge of people and places is represented separately in AT and PM areas, whereas hippocampus represents semantic knowledge of both categories.SIGNIFICANCE STATEMENT Humans acquire detailed semantic knowledge about people (e.g., their occupation and personality) and places (e.g., their cultural or historical significance). While research has demonstrated that brain regions preferentially respond to pictures of people and places, less is known about whether these regions preferentially represent semantic knowledge about specific people and places. We used machine learning techniques to develop a model of semantic similarity based on information available from Wikipedia, validating the model against similarity ratings from human participants. Using our computational model, we found that semantic knowledge about people and places is represented in distinct anterior temporal and posterior medial brain networks, respectively. We further found that hippocampus, an important memory center, represented semantic knowledge for both types of stimuli.