The neural correlates of ongoing conscious thought

Abstract

A core goal in cognitive neuroscience is identifying the physical substrates of the patterns of thought that occupy our daily lives. Contemporary views suggest that the landscape of ongoing experience is heterogeneous and can be influenced by features of both the person and the context. This perspective piece considers recent work that explicitly accounts for both the heterogeneity of the experience and context dependence of patterns of ongoing thought. These studies reveal that systems linked to attention and control are important for organizing experience in response to changing environmental demands. These studies also establish a role of the default mode network beyond task-negative or purely episodic content, for example, implicating it in the level of vivid detail in experience in both task contexts and in spontaneous self-generated experiential states. Together, this work demonstrates that the landscape of ongoing thought is reflected in the activity of multiple neural systems, and it is important to distinguish between processes contributing to how the experience unfolds from those linked to how these experiences are regulated.

Keywords: Cognitive Neuroscience; Psychology; Techniques in Neuroscience.

Figure 1

Heterogeneity in the patterns of ongoing thought Upper panel. Using experience sampling to understanding patterns of experience. Ongoing experience varies across people, places, and time. Studies use experience sampling to gain better insight into the patterns of experience that are common in different individuals and in different situations, including in daily life. These can be related to objective behavioral and neural signatures recorded under laboratory conditions to help understand the neural contributions to different patterns of ongoing thought. Lower panel. Consistency in the latent structure of thought patterns as revealed through the decomposition of multi-dimensional experience sampling (MDES) data. The left-hand panel shows the results of the application of the same decomposition algorithm (principal components analysis, PCA) to sets of experience sampling questions recorded in different situations. It can be seen that this approach reveals a similar structure in reports across situations and that this structure is correlated across individuals. In this figure, the word clouds show the importance of the item through the font size (bigger = more important) and the direction of the association through the color (warmer colors = positive, cooler colors = negative).

Figure 2

Neural regions dissociating external task focus and states of episodic social cognition reflect opposing ends of a task-positive hierarchy Studies highlight that regions which are active during external task focus (shown in blue) and during self-generated episodic social thought (shown in red) fall at opposing sides of a neural hierarchy that describes the brain response to external tasks. The top left panel shows greater neural activity within the ventral medial prefrontal cortex when individuals engage in social episodic thought (Konu et al., 2020). The top right panel shows regions of the intra-parietal sulcus exhibiting greater activation when individuals are engaged in external task focus (Turnbull et al., 2019a). The word clouds describe the experience patterns associated with each pattern of neural response. The middle and lower panel shows the functional connectivity of these two regions (colored appropriately), and it can be seen that the distribution of these maps parallel a dimension in connectivity space which describes the brain response to increasing task demands from the study by (Margulies et al., 2016). The right-hand subpanel shows a region of the lateral fusiform cortex that shows greater activity when viewing faces for individuals who spent more time engaged in off-task thought in a separate laboratory session.

Figure 3

Regions of the posterior cingulate cortex are implicated in reports of vivid detailed thought across a range of states The top panel (colored blue) shows evidence of the role of the DMN, and in particular a region of posterior cingulate, in detailed task-relevant cognition during working memory. In a study measuring neural activity in conjunction with subjective reports of ongoing thought patterns, a region of the posterior cingulate cortex was identified that exhibited a stronger positive association with reports of detailed task-relevant experience during working memory than in a less demanding task variant (Turnbull et al., 2019b). In an individual difference study in which participants performed a similar paradigm in the laboratory and brain activity was recorded at rest, individuals who reported high levels of external detail during task performance in the lab exhibited greater functional connectivity between the default mode network and regions of the visual cortex (Turnbull et al., 2019b). The middle panel (colored green) shows greater activity in regions of the posterior cingulate cortex during self-reference for participants who maintained high levels of detail in a separate laboratory session (Murphy et al., 2019b). The lower panel (colored red) shows the results of a canonical correlation analysis highlighting neural regions, including the posterior cingulate cortex, as linked to both expertise in semantic processing and patterns of ongoing thought characterized by vivid mental time travel. Note the different associations between the term “task” and “detail” in the upper and lower word clouds in this figure, which imply that these states share high levels of detail but differ with respect to whether they refer to detailed task-relevant cognition or detailed self-generated thought.

Figure 4

Studies have highlighted the role of the ventral attention network (VAN) and in particular region BA 9/46 in the dorsolateral prefrontal cortex as important in regulating patterns of ongoing thought to ensure that they are appropriate given the demands imposed by the external environment The left panel shows the neural correlates of context regulation. Activity within a region of the left dorsolateral prefrontal cortex (shown in red) is associated with social-episodic thought when task demands are low and task focus when task demands are higher (Turnbull and et al., 2019a). The middle panel shows the functional architecture supporting better context regulation. Individuals who show better alignment of cognition with task demands in the laboratory show greater connectivity between the VAN (shown in purple) with a region of the left motor cortex (shown in yellow) at rest (Turnbull et al., 2019b). The lower right subpanel shows that a similar region of left motor cortex connectivity at rest is associated with greater levels of intentional mind wandering (Golchert et al., 2017) that maybe the hallmark of more contextually regulated ongoing thought (Seli et al., 2016).

Figure 5

Dynamic features of ongoing experience reflect the role of task-related hierarchies as an organizing framework for differentiating patterns of thought Analysis of the distribution of naturally occurring neural states at rest show that these hidden states tend to cluster toward the extreme ends of each of three well-described neural hierarchies (Gradient 1 unimodal-transmodal, Gradient 2 visual-motor, and Gradient 3 task-positive/task negative). Top left panel shows that states identified using hidden Markov modeling (HMM) tend to fall outside the region that corresponds to the distribution of synthetic states (indicated as contour plots and generated via permutation testing). The middle top panel shows the spatial motifs of two states identified that had multivariate associations with patterns of ongoing experience (displayed as word clouds). These broadly correspond to a state of unpleasant rumination and future planning. The histogram highlights that these states were differentiated along a connectivity gradient that resembles the effect of task demands on cognition (gradient 3). It is also possible to explore the dynamics of ongoing thought using experience sampling in a task. States of on-task thought tend to decline over time, and this phenomenon can be visualized by calculating the similarity in spatial maps that describe neural processes that changes with time during task performance and relating these to spatial maps which describe the difference between being on task or focused on social episodic states. These are presented in the lower middle panel of this figure. The lower right plot shows that both maps associated with being on task or engaged in social episodic thought occupy opposing sides of gradient 3. Neural estimations of regions that change the most with time occupy similar positions on the same dimension (regions that decrease the most are closer to the on-task state, while regions that increase the most with time are close to the social episodic patterns).