Matthew L. Dixon

Improved modulation of rostrolateral prefrontal cortex using real-time fMRI training and meta-cognitive awareness

Recent real-time fMRI (rt-fMRI) training studies have demonstrated that subjects can achieve improved control over localized brain regions by using real-time feedback about the level of fMRI signal in these regions. It has remained unknown, however, whether subjects can gain control over anterior prefrontal cortex (PFC) regions that support some of the most complex forms of human thought. In this study, we used rt-fMRI training to examine whether subjects can learn to regulate the rostrolateral prefrontal cortex (RLPFC), or the lateral part of the anterior PFC, by using a meta-cognitive awareness strategy. We show that individuals can achieve improved regulation over the level of fMRI signal in their RLPFC by turning attention towards or away from their own thoughts. The ability to achieve improved modulation was contingent on observing veridical real-time feedback about the level of RLPFC activity during training; a sham-feedback control group demonstrated no improvement in modulation ability and neither did control subjects who received no rt-fMRI feedback but underwent otherwise identical training. Prior to training, meta-cognitive awareness was associated with recruitment of anterior PFC subregions, including both RLPFC and medial PFC, as well as a number of other midline and posterior cortical regions. Following training, however, regulation improvement was specific to RLPFC and was not observed in other frontal, midline, or parietal cortical regions. These results demonstrate the feasibility of acquiring control over high-level prefrontal regions through rt-fMRI training and offer a novel view into the correspondence between observable neuroscientific measures and highly subjective mental states.

A framework for understanding the relationship between externally and internally directed cognition.

Externally directed cognition (EDC) involves attending to stimuli in the external environment, whereas internally directed cognition (IDC) involves attending internally to thoughts, memories and mental imagery. To date, most studies have focused on the competition or trade-offs between these modes of cognition. However, both EDC and IDC include a variety of cognitive states that differ along multiple dimensions. These dimensions may influence the way in which EDC and IDC relate to each other. In this review, we present a novel framework that considers whether cognitive resources are oriented externally or internally, and also whether a given cognitive state involves intentional (i.e., voluntary) or spontaneous (i.e., involuntary) processing. Within this framework, we examine the conditions under which EDC and IDC are expected to either compete, or co-occur without interference. We argue that EDC and IDC are not inherently antagonistic, but when both involve higher levels of intentionality they are increasingly likely to compete, due to the capacity limitations of intentional processing. In contrast, if one or both involve spontaneous processing, EDC and IDC can co-occur with minimal interference given that involuntary processes are not subject to the same capacity constraints. A review of the brain regions implicated in EDC and IDC suggests that their neural substrates are partially segregated and partially convergent. Both EDC and IDC recruit the lateral prefrontal cortex (PFC) during intentional processing, and may therefore compete over the processes and representational space it supports. However, at lower levels of intentionality, EDC and IDC rely on largely distinct neural structures, which may enable their co-occurrence without interference. The proposal that EDC and IDC can in some cases co-occur, provides a framework for understanding the complex mental states that underlie theory of mind, creativity, the influence of self-evaluative processing on cognitive control, and memory-guided attention.

Functional neuroanatomy of meditation: A review and meta-analysis of 78 functional neuroimaging investigations

Meditation is a family of mental practices that encompasses a wide array of techniques employing distinctive mental strategies. We systematically reviewed 78 functional neuroimaging (fMRI and PET) studies of meditation, and used activation likelihood estimation to meta-analyze 257 peak foci from 31 experiments involving 527 participants. We found reliably dissociable patterns of brain activation and deactivation for four common styles of meditation (focused attention, mantra recitation, open monitoring, and compassion/loving-kindness), and suggestive differences for three others (visualization, sense-withdrawal, and non-dual awareness practices). Overall, dissociable activation patterns are congruent with the psychological and behavioral aims of each practice. Some brain areas are recruited consistently across multiple techniques-including insula, pre/supplementary motor cortices, dorsal anterior cingulate cortex, and frontopolar cortex-but convergence is the exception rather than the rule. A preliminary effect-size meta-analysis found medium effects for both activations (d=0.59) and deactivations (d=-0.74), suggesting potential practical significance. Our meta-analysis supports the neurophysiological dissociability of meditation practices, but also raises many methodological concerns and suggests avenues for future research.

The lateral prefrontal cortex and complex value-based learning and decision making.

Tremendous progress has been made in discerning the neurocognitive basis of value-based decision making and learning. Although the majority of studies to date have employed simple task paradigms, recent work has started to examine more complex aspects of value processing including: the value of engaging rule-based cognitive control; the integration of multiple pieces of information (e.g., reward magnitude and delay) to discern the best course of action; pursuing future rewards; valuation of abstract concepts (e.g., fairness); and comparing the value of executed versus imagined alternative actions. We provide a comprehensive review of functional neuroimaging, electrophysiological, and lesion evidence suggesting that the lateral prefrontal cortex (LPFC) plays a critical role in these complex aspects of value processing. In particular, we focus on the specific information that the LPFC represents, and argue that it includes both cognitive and value-based information. We also discuss how the role of the LPFC is distinct from other value-related regions. Finally, we articulate a framework for understanding the contribution of subregions along the rostro-caudal axis of the LPFC, and thereby bridge the cognitive control and decision making literatures.

Dynamics of neural recruitment surrounding the spontaneous arising of thoughts in experienced mindfulness practitioners

Thoughts arise spontaneously in our minds with remarkable frequency, but tracking the brain systems associated with the early inception of a thought has proved challenging. Here we addressed this issue by taking advantage of the heightened introspective ability of experienced mindfulness practitioners to observe the onset of their spontaneously arising thoughts. We found subtle differences in timing among the many regions typically recruited by spontaneous thought. In some of these regions, fMRI signal peaked prior to the spontaneous arising of a thought - most notably in the medial temporal lobe and inferior parietal lobule. In contrast, activation in the medial prefrontal, temporopolar, mid-insular, lateral prefrontal, and dorsal anterior cingulate cortices peaked together with or immediately following the arising of spontaneous thought. We propose that brain regions that show antecedent recruitment may be preferentially involved in the initial inception of spontaneous thoughts, while those that show later recruitment may be preferentially involved in the subsequent elaboration and metacognitive processing of spontaneous thoughts. Our findings highlight the temporal dynamics of neural recruitment surrounding the emergence of spontaneous thoughts and may help account for some of spontaneous thoughts peculiar qualities, including its wild diversity of content and its links to memory and attention.

Interactions between the default network and dorsal attention network vary across default subsystems, time, and cognitive states

ABSTRACT Anticorrelation between the default network (DN) and dorsal attention network (DAN) is thought to be an intrinsic aspect of functional brain organization reflecting competing functions. However, the effect size of functional connectivity (FC) between the DN and DAN has yet to be established. Furthermore, the stability of anticorrelations across distinct DN subsystems, different contexts, and time, remains unexplored. In study 1 we summarize effect sizes of DN‐DAN FC from 20 studies, and in study 2 we probe the variability of DN‐DAN interactions across six different cognitive states in a new data set. We show that: (i) the DN and DAN have an independent rather than anticorrelated relationship when global signal regression is not used (median effect size across studies: r=−.06; 95% CI: −.15 to .08); (ii) the DAN exhibits weak negative FC with the DN Core subsystem but is uncorrelated with the dorsomedial prefrontal and medial temporal lobe subsystems; (iii) DN‐DAN interactions vary significantly across different cognitive states; (iv) DN‐DAN FC fluctuates across time between periods of anticorrelation and periods of positive correlation; and (v) changes across time in the strength of DN‐DAN coupling are coordinated with interactions involving the frontoparietal control network (FPCN). Overall, the observed weak effect sizes related to DN‐DAN anticorrelation suggest the need to re‐conceptualize the nature of interactions between these networks. Furthermore, our findings demonstrate that DN‐DAN interactions are not stable, but rather, exhibit substantial variability across time and context, and are coordinated with broader network dynamics involving the FPCN.

Emotion and the Prefrontal Cortex: An Integrative Review.

The prefrontal cortex (PFC) plays a critical role in the generation and regulation of emotion. However, we lack an integrative framework for understanding how different emotion-related functions are organized across the entire expanse of the PFC, as prior reviews have generally focused on specific emotional processes (e.g., decision making) or specific anatomical regions (e.g., orbitofrontal cortex). Additionally, psychological theories and neuroscientific investigations have proceeded largely independently because of the lack of a common framework. Here, we provide a comprehensive review of functional neuroimaging, electrophysiological, lesion, and structural connectivity studies on the emotion-related functions of 8 subregions spanning the entire PFC. We introduce the appraisal-by-content model, which provides a new framework for integrating the diverse range of empirical findings. Within this framework, appraisal serves as a unifying principle for understanding the PFC’s role in emotion, while relative content-specialization serves as a differentiating principle for understanding the role of each subregion. A synthesis of data from affective, social, and cognitive neuroscience studies suggests that different PFC subregions are preferentially involved in assigning value to specific types of inputs: exteroceptive sensations, episodic memories and imagined future events, viscero-sensory signals, viscero-motor signals, actions, others’ mental states (e.g., intentions), self-related information, and ongoing emotions. We discuss the implications of this integrative framework for understanding emotion regulation, value-based decision making, emotional salience, and refining theoretical models of emotion. This framework provides a unified understanding of how emotional processes are organized across PFC subregions and generates new hypotheses about the mechanisms underlying adaptive and maladaptive emotional functioning.

Evidence for rostro-caudal functional organization in multiple brain areas related to goal-directed behavior

The functional organization of brain areas supporting goal-directed behavior is debated. Some accounts suggest a rostro-caudal organization, while others suggest a broad recruitment as part of a multiple demand network. We used fMRI and an anatomical region of interest (ROI) approach to test which account better characterizes the organization of key brain areas related to goal-directed behavior: the lateral prefrontal cortex (LPFC), medial prefrontal cortex (MPFC), cingulate cortex, and insula. Subjects performed a cognitive control task with distinct trial events corresponding to rule representation, rule maintenance, action execution, and monitoring progress towards an overarching motivational goal. The use of ROIs allowed us to look for evidence of rostro-caudal gradients during each event separately. Our results provide strong evidence for rostro-caudal gradients in all regions. During the action execution period, activation was robust in caudal ROIs and decreased linearly moving to rostral ROIs in the LPFC, cingulate cortex, and MPFC. Conversely, during the goal monitoring period, activation was weak in caudal ROIs and increased linearly moving to the rostral ROIs in the aforementioned regions. The insula exhibited the reverse pattern. These findings provide evidence for rostro-caudal organization in multiple regions within the same study. More importantly, they demonstrate that rostro-caudal gradients can be observed during individual trial events, ruling out confounding factors such as task difficulty.

Learning to ignore: Acquisition of sustained attentional suppression

We examined whether the selection mechanisms committed to the suppression of ignored stimuli can be modified by experience to produce a sustained, rather than transient, change in behavior. Subjects repeatedly ignored the shape of stimuli, while attending to their color. On subsequent attention to shape, there was a robust and sustained decrement in performance that was selective to when shape was ignored across multiple-colortarget contexts, relative to a single-color-target context. Thus, amount of time ignored was not sufficient to induce a sustained performance decrement. Moreover, in this group, individual differences in initial color target selection were associated with the subsequent performance decrement when attending to previously ignored stimuli. Accompanying this sustained decrement in performance was a transfer in the locus of suppression from an exemplar (e.g., a circle) to a feature (i.e., shape) level of representation. These data suggest that learning can influence attentional selection by sustained attentional suppression of ignored stimuli.

Cognitive control, emotional value, and the lateral prefrontal cortex

Cognitive control refers to the intentional selection of thoughts, emotions, and behaviors based on current task demands and social context, and the concomitant suppression of inappropriate habitual actions (Miller and Cohen, 2001). Common situations that require cognitive control include: studying for an exam while resisting the impulse to check Facebook; having fruit instead of dessert when on a diet; and being patient with ones kids instead of yelling at them for spilling juice on the carpet. Historically, there has been preferential interest in how cognitive control operates. An influential model suggests that the lateral prefrontal cortex (LPFC) represents rules or instructions in working memory and that this information adaptively guides perceptual and motor processing in posterior brain regions, thus resulting in the selection of appropriate behaviors, and the suppression of maladaptive habitual actions (Miller and Cohen, 2001; Bunge, 2004). Surprisingly, there has been less focus on why individuals choose to engage cognitive control in the first place (Dixon and Christoff, 2012; Botvinick and Braver, 2015). In this article, I outline a value-based framework of cognitive control which suggests that: (1) individuals choose to engage cognitive control when they expect that it will produce an emotionally valued outcome (i.e., a reward or the avoidance of punishment); (2) the LPFC is a critical neural substrate involved in representing the value of engaging cognitive control; and (3) the LPFC is organized along a rostro-caudal axis, with different sub-regions contributing to different elements of the decision to employ cognitive control.