Nonlinear Feedback Modulation of Saccade Choice on Neural Processes During Flexible Decision-Making

核心概念

Sensory evaluation and action selection processes in the primate brain nonlinearly interact during flexible decision-making, mediated by precise feedback connectivity between the neural circuits underlying these distinct processes.

要約

The study examined the interplay between sensory evaluation and action selection processes in the posterior parietal cortex (PPC) of primates performing a flexible visual-motion discrimination task. The authors found that the neural activity in PPC related to the evaluation of visual motion stimuli was nonlinearly modulated by the monkeys' following saccade choices, even though the saccade targets were located outside the neurons' response fields.
This nonlinear feedback modulation was aligned with the functional properties of individual neurons and specifically impacted the decision-correlated but not the stimulus-correlated activity in PPC. Computational modeling using multi-module recurrent neural networks (RNNs) replicated the key findings from the neurophysiology experiments, and further revealed that the selectivity-specific feedback connections between the neural modules encoding sensory evaluation and action selection were crucial for mediating this modulation.
The feedback modulation enhanced the consistency of flexible decisions by strengthening the attractor basins of the network dynamics underlying saccade choices. These results highlight an iterative computation between distinct neural processes of decision-making, mediated primarily by precise feedback connectivity, which contributes to the optimization of flexible decision-making.

統計

"As the motion coherence increased, both monkeys chose the correct target more frequently and more rapidly."
"LIP neurons showed significantly elevated activity in the contralateral target (CT) relative to the ipsilateral target (IT) condition at all coherence levels during presentation of their preferred motion direction."
"The decision-related component of LIP direction selectivity was significantly greater in the CT condition than in the IT condition."

引用

"Sensory evaluation and action selection emerge as two fundamental processes essential for implementing perceptual decision behavior."
"Neural activity related to sensory evaluation and action selection overlaps temporally and spatially in the brain, leaving open the possibility of interplay between these distinct processes during decision-making."
"The precise feedback connections between units that showed matched functional properties within different network modules were the key circuit mechanism for mediating the modulation of sensory evaluation by action selection."

抽出されたキーインサイト

Nonlinear feedback modulation contributes to the optimization of flexible decision-making

by Zhou,Y., Wu,... 場所 www.biorxiv.org 07-18-2023

https://www.biorxiv.org/content/10.1101/2023.07.15.549136v2

深掘り質問

How might the selectivity-specific feedback connectivity emerge during learning and development, and what are the potential neural mechanisms underlying the formation of such precise feedback connections

The emergence of selectivity-specific feedback connectivity during learning and development likely involves a combination of experience-dependent plasticity mechanisms and Hebbian learning principles. Initially, during early stages of development, there may be a random and diffuse pattern of feedback connections between different neural ensembles involved in sensory evaluation and action selection processes. As the organism interacts with the environment and learns to make decisions based on sensory inputs, these connections could undergo refinement through activity-dependent processes.
One potential mechanism underlying the formation of precise feedback connections is spike-timing-dependent plasticity (STDP), where the timing of pre- and postsynaptic action potentials determines the strength of synaptic connections. Neurons that fire together frequently may strengthen their connections, leading to the development of selectivity-specific feedback pathways between neural ensembles encoding related information. Additionally, homeostatic plasticity mechanisms could help maintain the stability and balance of these connections over time.
Furthermore, the organization of feedback connections could be influenced by topographic mapping and functional segregation within neural circuits. Neurons with similar response properties or encoding preferences may establish stronger connections with each other, creating a network of selectivity-specific feedback pathways. This organization could be guided by molecular cues, such as cell adhesion molecules, that help neurons recognize and form connections with specific partners based on their functional properties.
Overall, the emergence of selectivity-specific feedback connectivity likely involves a dynamic interplay between experience-driven plasticity mechanisms, Hebbian learning principles, and molecular guidance cues, leading to the formation of precise and functionally relevant feedback pathways in the brain.

What are the potential limitations of the current experimental design and computational modeling approach, and how could future studies address these limitations to further elucidate the neural mechanisms of flexible decision-making

The current experimental design and computational modeling approach have several potential limitations that future studies could address to further elucidate the neural mechanisms of flexible decision-making:

Limited Neural Circuit Complexity: The current models focus on specific brain regions and simplified neural circuits. Future studies could incorporate more complex and interconnected neural networks to better capture the distributed nature of decision-making processes in the brain.

Simplified Task Paradigm: The FVMD task used in the experiments may not fully capture the complexity of real-world decision-making scenarios. Future studies could design tasks that involve more nuanced decision processes and incorporate multiple sensory modalities to better mimic natural decision-making contexts.

Static Feedback Connectivity: The current models assume fixed feedback connections between neural ensembles. Future studies could explore dynamic feedback mechanisms that adapt and change over time based on ongoing sensory inputs and behavioral outcomes.

Lack of Behavioral Validation: While the RNN models replicate neural activity patterns, there is a need for behavioral validation to ensure that the models accurately capture decision-making behaviors. Future studies could integrate behavioral data to validate the computational models.

Limited Understanding of Plasticity Mechanisms: The exact mechanisms underlying the formation and plasticity of feedback connections are not fully understood. Future research could delve deeper into the molecular and cellular processes that govern synaptic plasticity and connectivity changes in decision-making circuits.

By addressing these limitations, future studies can provide a more comprehensive understanding of the neural mechanisms underlying flexible decision-making and enhance the translational relevance of the findings.

Given the importance of feedback modulation in optimizing decision-making, how might disruptions in feedback connectivity contribute to decision-making deficits observed in neurological and psychiatric disorders

Disruptions in feedback connectivity could play a significant role in decision-making deficits observed in neurological and psychiatric disorders. Here are some ways in which disruptions in feedback connectivity may contribute to decision-making deficits:

Impaired Information Integration: Alterations in feedback connections may lead to difficulties in integrating sensory information with prior knowledge and internal representations, affecting the accuracy and efficiency of decision-making processes.

Reduced Decision Consistency: Disruptions in feedback modulation could result in unstable neural dynamics and shallow attractor basins, leading to increased decision variability and reduced decision consistency in individuals with neurological or psychiatric disorders.

Dysfunctional Learning and Adaptation: Feedback connectivity is crucial for learning from outcomes and adapting behavior based on feedback. Deficits in feedback mechanisms could impair the ability to update decision strategies and learn from experience, contributing to maladaptive decision-making behaviors.

Cognitive Flexibility Deficits: Feedback connections are essential for cognitive flexibility and the ability to switch between different decision strategies. Disruptions in feedback modulation may lead to rigidity in decision-making processes and difficulties in adapting to changing task demands.

Contributing to Symptomatology: In disorders such as schizophrenia or autism spectrum disorders, disruptions in feedback connectivity may contribute to cognitive symptoms related to decision-making deficits, such as impaired social cognition or difficulties in interpreting and responding to environmental cues.

Understanding how disruptions in feedback connectivity impact decision-making processes in neurological and psychiatric disorders could provide insights into the underlying neural mechanisms and inform the development of targeted interventions to improve decision-making abilities in affected individuals.