Brain dynamics and spatiotemporal trajectories during threat processing

Reviewer #1 (Public review):

Summary:

The manuscript uses state-of-the-art analysis technology to document the spatio-temporal dynamics of brain activity during the processing of threats. The authors offer convincing evidence that complex spatio-temporal aspects of brain dynamics are essential to describe brain operations during threat processing.

Strengths:

Rigorous complex analyses well suited to the data.

Weaknesses:

Lack of a simple take-home message about discovery of a new brain operation.

Reviewer #2 (Public review):

Summary:

This paper by Misra and Pessoa uses switching linear dynamical systems (SLDS) to investigate the neural network dynamics underlying threat processing at varying levels of proximity. Using an existing dataset from a threat-of-shock paradigm in which threat proximity is manipulated in a continuous fashion, the authors first show that they can identify states that each has their own linear dynamical system and are consistently associated with distinct phases of the threat-of-shock task (e.g., "peri-shock", "not near", etc). They then show how activity maps associated with these states are in agreement with existing literature on neural mechanisms of threat processing, and how activity in underlying brain regions alters around state transitions. The central novelty of the paper lies in its analyses of how intrinsic and extrinsic factors contribute to within-state trajectories and between-state transitions. A final set of analyses shows how the findings generalize to another (related) threat paradigm.

Strengths:

The analyses for this study are conducted at a very high level of mathematical and theoretical sophistication. The paper is very well written and effectively communicates complex concepts from dynamical systems. I am enthusiastic about this paper, but I think the authors have not yet exploited the full potential of their analyses in making this work meaningful toward increasing our neuroscientific understanding of threat processing, as explained below.

Weaknesses:

(1) I appreciate the sophistication of the analyses applied and/or developed by the authors. These methods have many potential use cases for investigating the network dynamics underlying various cognitive and affective processes. However, I am somewhat disappointed by the level of inferences made by the authors based on these analyses at the level of systems neuroscience. As an illustration consider the following citations from the abstract: "The results revealed that threat processing benefits from being viewed in terms of dynamic multivariate patterns whose trajectories are a combination of intrinsic and extrinsic factors that jointly determine how the brain temporally evolves during dynamic threat" and "We propose that viewing threat processing through the lens of dynamical systems offers important avenues to uncover properties of the dynamics of threat that are not unveiled with standard experimental designs and analyses". I can agree to the claim that we may be able to better describe the intrinsic and extrinsic dynamics of threat processing using this method, but what is now the contribution that this makes toward understanding these processes?

(2) How sure can we be that it is possible to separate extrinsically and intrinsically driven dynamics?