Dissociable Neural Systems Research Articles

Partisans process policy-based and identity-based messages using dissociable neural systems.

Political partisanship is often conceived as a lens through which people view politics. Behavioral research has distinguished two types of "partisan lenses"-policy-based and identity-based-that may influence peoples' perception of political events. Little is known, however, about the mechanisms through which partisan discourse appealing to policy beliefs or targeting partisan identities operate within individuals. We addressed this question by collecting neuroimaging data while participants watched videos of speakers expressing partisan views. A "partisan lens effect" was identified as the difference in neural synchrony between each participant's brain response and that of their partisan ingroup vs. outgroup. When processing policy-based messaging, a partisan lens effect was observed in socio-political reasoning and affective responding brain regions. When processing negative identity-based attacks, a partisan lens effect was observed in mentalizing and affective responding brain regions. These data suggest that the processing of political discourse that appeals to different forms of partisanship is supported by related but distinguishable neural-and therefore psychological-mechanisms, which may have implications for how we characterize partisanship and ameliorate its deleterious impacts.

The Neural Corelates of Constructing Conceptual and Perceptual Representations of Autobiographical Memories.

Contemporary neurocognitive frameworks propose that conceptual and perceptual content of autobiographical memories-personal past experiences-are processed by dissociable neural systems. Other work has proposed a central role of the anterior hippocampus in initially constructing autobiographical memories, regardless of the content. Here, we report on an fMRI study that utilized a repeated retrieval paradigm to test these ideas. In an MRI scanner, participants retrieved autobiographical memories at three timepoints. During the third retrieval, participants either shifted their focus to the conceptual content of the memory, the perceptual content of the memory, or retrieved the memory as they had done so on previous trials. We observed stronger anterior hippocampal activity for the first retrieval compared with later retrievals, regardless of whether there was a shift in content in those later trials. We also found evidence for separate cortical systems when constructing autobiographical memories with a focus on conceptual or perceptual content. Finally, we found that there was common engagement between later retrievals that required a shift toward conceptual content and the initial retrieval of a memory. This final finding was explored further with a behavioral experiment that provided evidence that focusing on conceptual content of a memory guides memory construction, whereas perceptual content adds precision to a memory. Together, these findings suggest there are distinct content-oriented cortical systems that work with the anterior hippocampus to construct representations of autobiographical memories.

Deconstructing Mechanisms of Motivational Impairment Transdiagnostically

Motivation is a multifaceted construct that includes processes related to experiencing pleasure, anticipating pleasure, effort allocation, and the generation of action plans, each associated with dissociable neural systems. We used data from four studies to examine the relative associations to symptom domains within across diagnostic categories.

Dissociable Neural Systems Support the Learning and Transfer of Hierarchical Control Structure.

Humans can draw insight from previous experiences to quickly adapt to novel environments that share a common underlying structure. Here we combine functional imaging and computational modeling to identify the neural systems that support the discovery and transfer of hierarchical task structure. Human subjects (male and female) completed multiple blocks of a reinforcement learning task that contained a global hierarchical structure governing stimulus-response action mapping. First, behavioral and computational evidence showed that humans successfully discover and transfer the hierarchical rule structure embedded within the task. Next, analysis of fMRI BOLD data revealed activity across a frontoparietal network that was specifically associated with the discovery of this embedded structure. Finally, activity throughout a cingulo-opercular network supported the transfer and implementation of this discovered structure. Together, these results reveal a division of labor in which dissociable neural systems support the learning and transfer of abstract control structures.SIGNIFICANCE STATEMENT A fundamental and defining feature of human behavior is the ability to generalize knowledge from the past to support future action. Although the neural circuits underlying more direct forms of learning have been well established over the last century, we still lack a solid framework from which to investigate more abstract, higher-order human learning and knowledge generalization. We designed a novel behavioral paradigm to specifically isolate a learning process in which previous knowledge, rather than directly indicating the correct action, instead guides the search for the correct action. Moreover, we identify that this learning process is achieved via the coordinated and temporally specific activity of two prominent cognitive control brain networks.

Dissociable neural systems for unconditioned acute and sustained fear

Fear protects organisms by increasing vigilance and preparedness, and by coordinating survival responses during life-threatening encounters. The fear circuit must thus operate on multiple timescales ranging from preparatory sustained alertness to acute fight-or-flight responses. Here we studied the brain basis of sustained and acute fear using naturalistic functional magnetic resonance imaging (fMRI) enabling analysis of different time-scales of fear responses. Subjects (N ​= ​37) watched feature-length horror movies while their hemodynamic brain activity was measured with fMRI. Time-variable intersubject correlation (ISC) was used to quantify the reliability of brain activity across participants, and seed-based phase synchronization was used for characterizing dynamic connectivity. Subjective ratings of fear were used to assess how synchronization and functional connectivity varied with emotional intensity. These data suggest that acute and sustained fear are supported by distinct neural pathways, with sustained fear amplifying mainly sensory responses, and acute fear increasing activity in brainstem, thalamus, amygdala and cingulate cortices. Sustained fear increased ISC in regions associated with acute fear, and also amplified functional connectivity within this network. The results were replicated in an independent experiment with a different subject sample and stimulus movie. The functional interplay between cortical networks involved in sustained anticipation of, and acute response to, threat involves a complex and dynamic interaction that depends on the proximity of threat, and the need to employ threat appraisals and vigilance for decision making and response selection.

Blockade of dopamine D1 receptors in male rats disrupts morphine reward in pain naïve but not in chronic pain states.

The rewarding effect of opiates is mediated through dissociable neural systems in drug naïve and drug-dependent states. Neuroadaptations associated with chronic drug use are similar to those produced by chronic pain, suggesting that opiate reward could also involve distinct mechanisms in chronic pain and pain-naïve states. We tested this hypothesis by examining the effect of dopamine (DA) antagonism on morphine reward in a rat model of neuropathic pain.Neuropathic pain was induced in male Sprague-Dawley rats through chronic constriction (CCI) of the sciatic nerve; reward was assessed in the conditioned place preference (CPP) paradigm in separate groups at early (4-8 days post-surgery) and late (11-15 days post-surgery) phases of neuropathic pain. Minimal effective doses of morphine that produced a CPP in early and late phases of neuropathic pain were 6 mg/kg and 2 mg/kg respectively. The DA D1 receptor antagonist, SCH23390, blocked a morphine CPP in sham, but not CCI, rats at a higher dose (0.5 mg/kg), but had no effect at a lower dose (0.1 mg/kg). The DA D2 receptor antagonist, eticlopride (0.1 and 0.5 mg/kg), had no effect on a morphine CPP in sham or CCI rats, either in early or late phases of neuropathic pain. In the CPP paradigm, morphine reward involves DA D1 mechanisms in pain-naïve but not chronic pain states. This could reflect increased sensitivity to drug effects in pain versus no pain conditions and/or differential mediation of opiate reward in these two states.

There Is More Than One Kind of Extinction Learning.

The view that different kinds of memory are mediated by dissociable neural systems has received extensive experimental support. Dissociations between memory systems are usually observed during initial acquisition, consolidation, and retrieval of memory, however increasing evidence also indicates a role for multiple memory systems in extinction behavior. The present article reviews a recent series of maze learning experiments that provide evidence for a multiple memory systems approach to extinction learning and memory. Evidence is described indicating that: (1) the hippocampus and dorsolateral striatum (DLS) mediate different kinds of extinction learning; (2) the effectiveness of different extinction protocols depends on the kind of memory being extinguished; and (3) whether a neural system is involved in extinction is also determined by the extinction protocol and kind of memory undergoing extinction. Based on these findings, a novel hypothetical model regarding the role of multiple memory systems in extinction is presented. In addition, the relevance of this multiple memory systems approach to other learning paradigms involving extinction (i.e., extinction of conditioned fear) and for treating human psychopathologies characterized by maladaptive memories (e.g., drug addiction and relapse) is briefly considered.

Neural correlates of attentional capture by stimuli previously associated with social reward

ABSTRACTOur attention is strongly influenced by reward learning. Stimuli previously associated with monetary reward have been shown to automatically capture attention in both behavioral and neurophysiological studies. Stimuli previously associated with positive social feedback similarly capture attention; however, it is unknown whether such social facilitation of attention relies on similar or dissociable neural systems. Here, we used the value-driven attentional capture paradigm in an fMRI study to identify the neural correlates of attention to stimuli previously associated with social reward. The results reveal learning-dependent priority signals in the contralateral visual cortex, posterior parietal cortex, and caudate tail, similar to studies using monetary reward. An additional priority signal was consistently evident in the right middle frontal gyrus (MFG). Our findings support the notion of a common neural mechanism for directing attention on the basis of selection history that generalizes across different types of reward.

Dissociable Neural Systems for Recognizing Places and Navigating through Them.

When entering an environment, we can use the present visual information from the scene to either recognize the kind of place it is (e.g., a kitchen or a bedroom) or navigate through it. Here we directly test the hypothesis that these two processes, what we call "scene categorization" and "visually-guided navigation", are supported by dissociable neural systems. Specifically, we manipulated task demands by asking human participants (male and female) to perform a scene categorization, visually-guided navigation, and baseline task on images of scenes, and measured both the average univariate responses and multivariate spatial pattern of responses within two scene-selective cortical regions, the parahippocampal place area (PPA) and occipital place area (OPA), hypothesized to be separably involved in scene categorization and visually-guided navigation, respectively. As predicted, in the univariate analysis, PPA responded significantly more during the categorization task than during both the navigation and baseline tasks, whereas OPA showed the complete opposite pattern. Similarly, in the multivariate analysis, a linear support vector machine achieved above-chance classification for the categorization task, but not the navigation task in PPA. By contrast, above-chance classification was achieved for both the navigation and categorization tasks in OPA. However, above-chance classification for both tasks was also found in early visual cortex and hence not specific to OPA, suggesting that the spatial patterns of responses in OPA are merely inherited from early vision, and thus may be epiphenomenal to behavior. Together, these results are evidence for dissociable neural systems involved in recognizing places and navigating through them.SIGNIFICANCE STATEMENT It has been nearly three decades since Goodale and Milner demonstrated that recognizing objects and manipulating them involve distinct neural processes. Today we show the same is true of our interactions with our environment: recognizing places and navigating through them are neurally dissociable. More specifically, we found that a scene-selective region, the parahippocampal place area, is active when participants are asked to categorize a scene, but not when asked to imagine navigating through it, whereas another scene-selective region, the occipital place area, shows the exact opposite pattern. This double dissociation is evidence for dissociable neural systems within scene processing, similar to the bifurcation of object processing described by Goodale and Milner (1992).

Learning what to expect and when to expect it involves dissociable neural systems.

Two experiments with Long-Evans rats examined the potential independence of learning about different features of food reward, namely, "what" reward is to be expected and "when" it will occur. This was examined by investigating the effects of selective reward devaluation upon responding in an instrumental peak timing task in Experiment 1 and by exploring the effects of pre-training lesions targeting the basolateral amygdala (BLA) upon the selective reward devaluation effect and interval timing in a Pavlovian peak timing task in Experiment 2. In both tasks, two stimuli, each 60 s long, signaled that qualitatively distinct rewards (different flavored food pellets) could occur after 20 s. Responding on non-rewarded probe trials displayed the characteristic peak timing function with mean responding gradually increasing and peaking at approximately 20 s before more gradually declining thereafter. One of the rewards was then independently paired repeatedly with LiCl injections in order to devalue it whereas the other reward was unpaired with these injections. In a final set of test sessions in which both stimuli were presented without rewards, it was observed that responding was selectively reduced in the presence of the stimulus signaling the devalued reward compared to the stimulus signaling the still valued reward. Moreover, the timing function was mostly unaltered by this devaluation manipulation. Experiment 2 showed that pre-training BLA lesions abolished this selective reward devaluation effect, but it had no impact on peak timing functions shown by the two stimuli. It appears from these data that learning about "what" and "when" features of reward may entail separate underlying neural systems.

Neurological, nutritional and alcohol consumption factors underlie cognitive and motor deficits in chronic alcoholism.

Variations in pattern and extent of cognitive and motor impairment occur in alcoholism (ALC). Causes of such heterogeneity are elusive and inconsistently accounted for by demographic or alcohol consumption differences. We examined neurological and nutritional factors as possible contributors to heterogeneity in impairment. Participants with ALC (n=96) and a normal comparison group (n=41) were examined on six cognitive and motor domains. Signs of historically determined subclinical Wernicke's encephalopathy were detected using the Caine et al. criteria, which were based on postmortem examination and chart review of antemortem data of alcoholic cases with postmortem evidence for Wernicke's encephalopathy. Herein, four Caine criteria provided quantification of dietary deficiency, cerebellar dysfunction, low general cognitive functioning and oculomotor abnormalities in 86 of the 96 ALC participants. Subgroups based on Caine criteria yielded a graded effect, where those meeting more criteria exhibited greater impairment than those meeting no to fewer criteria. These results could not be accounted for by history of drug dependence. Multiple regression indicated that compromised performance on ataxia, indicative of cerebellar dysfunction, predicted non-mnemonic and upper motor deficits, whereas low whole blood thiamine level, consistent with limbic circuit dysfunction, predicted mnemonic deficits. This double dissociation indicates biological markers that contribute to heterogeneity in expression of functional impairment in ALC. That non-mnemonic and mnemonic deficits are subserved by the dissociable neural systems of frontocerebellar and limbic circuitry, both commonly disrupted in ALC, suggests neural mechanisms that can differentially affect selective functions, thereby contributing to heterogeneity in pattern and extent of dysfunction in ALC.

Neural correlates of conventional and harm/welfare-based moral decision-making.

The degree to which social norms are processed by a unitary system or dissociable systems remains debated. Much research on children's social-cognitive judgments has supported the distinction between "moral" (harm/welfare-based) and "conventional" norms. However, the extent to which these norms are processed by dissociable neural systems remains unclear. To address this issue, 23 healthy participants were scanned with functional magnetic resonance imaging (fMRI) while they rated the wrongness of harm/welfare-based and conventional transgressions and neutral vignettes. Activation significantly greater than the neutral vignette baseline was observed in regions implicated in decision-making regions including rostral/ventral medial frontal, anterior insula and dorsomedial frontal cortices when evaluating both harm/welfare-based and social-conventional transgressions. Greater activation when rating harm/welfare-based relative to social-conventional transgressions was seen through much of ACC and bilateral inferior frontal gyrus. Greater activation was observed in superior temporal gyrus, bilateral middle temporal gyrus, left PCC, and temporal-parietal junction when rating social-conventional transgressions relative to harm/welfare-based transgressions. These data suggest that decisions regarding the wrongness of actions, irrespective of whether they involve care/harm-based or conventional transgressions, recruit regions generally implicated in affect-based decision-making. However, there is neural differentiation between harm/welfare-based and conventional transgressions. This may reflect the particular importance of processing the intent of transgressors of conventional norms and perhaps the greater emotional content or salience of harm/welfare-based transgressions.

A causal role for right frontopolar cortex in directed, but not random, exploration.

The explore-exploit dilemma occurs anytime we must choose between exploring unknown options for information and exploiting known resources for reward. Previous work suggests that people use two different strategies to solve the explore-exploit dilemma: directed exploration, driven by information seeking, and random exploration, driven by decision noise. Here, we show that these two strategies rely on different neural systems. Using transcranial magnetic stimulation to inhibit the right frontopolar cortex, we were able to selectively inhibit directed exploration while leaving random exploration intact. This suggests a causal role for right frontopolar cortex in directed, but not random, exploration and that directed and random exploration rely on (at least partially) dissociable neural systems.

Variation in the oxytocin receptor gene (OXTR) is associated with differences in moral judgment.

Moral judgments are produced through the coordinated interaction of multiple neural systems, each of which relies on a characteristic set of neurotransmitters. Genes that produce or regulate these neurotransmitters may have distinctive influences on moral judgment. Two studies examined potential genetic influences on moral judgment using dilemmas that reliably elicit competing automatic and controlled responses, generated by dissociable neural systems. Study 1 (N = 228) examined 49 common variants (SNPs) within 10 candidate genes and identified a nominal association between a polymorphism (rs237889) of the oxytocin receptor gene (OXTR) and variation in deontological vs utilitarian moral judgment (that is, judgments favoring individual rights vs the greater good). An association was likewise observed for rs1042615 of the arginine vasopressin receptor gene (AVPR1A). Study 2 (N = 322) aimed to replicate these findings using the aforementioned dilemmas as well as a new set of structurally similar medical dilemmas. Study 2 failed to replicate the association with AVPR1A, but replicated the OXTR finding using both the original and new dilemmas. Together, these findings suggest that moral judgment is influenced by variation in the oxytocin receptor gene and, more generally, that single genetic polymorphisms can have a detectable effect on complex decision processes.

The dissociable neural dynamics of cognitive conflict and emotional conflict control: An ERP study

This study investigated differences in the neural time-course of cognitive conflict and emotional conflict control, using event-related potentials (ERPs). Although imaging studies have provided some evidence that distinct, dissociable neural systems underlie emotional and nonemotional conflict resolution, no ERP study has directly compared these two types of conflict. Therefore, the present study used a modified face-word Stroop task to explore the electrophysiological correlates of cognitive and emotional conflict control. The behavioral data showed that the difference in response time of congruency (incongruent condition minus the congruent condition) was larger in the cognitive conflict task than in the emotional conflict task, which indicated that cognitive conflict was stronger than the emotional conflict in the present tasks. Analysis of the ERP data revealed a main effect of task type on N2, which may be associated with top-down attention. The N450 results showed an interaction between cognitive and emotional conflict, which might be related to conflict detection. In addition, we found the incongruent condition elicited a larger SP than the congruent condition, which might be related to conflict resolution.

Memory Systems and the Addicted Brain.

The view that anatomically distinct memory systems differentially contribute to the development of drug addiction and relapse has received extensive support. The present brief review revisits this hypothesis as it was originally proposed 20 years ago (1) and highlights several recent developments. Extensive research employing a variety of animal learning paradigms indicates that dissociable neural systems mediate distinct types of learning and memory. Each memory system potentially contributes unique components to the learned behavior supporting drug addiction and relapse. In particular, the shift from recreational drug use to compulsive drug abuse may reflect a neuroanatomical shift from cognitive control of behavior mediated by the hippocampus/dorsomedial striatum toward habitual control of behavior mediated by the dorsolateral striatum (DLS). In addition, stress/anxiety may constitute a cofactor that facilitates DLS-dependent memory, and this may serve as a neurobehavioral mechanism underlying the increased drug use and relapse in humans following stressful life events. Evidence supporting the multiple systems view of drug addiction comes predominantly from studies of learning and memory that have employed as reinforcers addictive substances often considered within the context of drug addiction research, including cocaine, alcohol, and amphetamines. In addition, recent evidence suggests that the memory systems approach may also be helpful for understanding topical sources of addiction that reflect emerging health concerns, including marijuana use, high-fat diet, and video game playing.

Emotional and cognitive dysregulation in schizophrenia and depression: understanding common and distinct behavioral and neural mechanisms

Emerging behavioral and neuroimaging studies in schizophrenia (SCZ) and major depressive disorder (MD) are mapping mechanisms of co-occurring and distinct affective disturbances across these disorders. This constitutes a critical goal towards developing rationally guided therapies for upstream neural pathways that contribute to comorbid symptoms across disorders. We highlight the current state of the art in our understanding of emotional dysregulation in SCZ versus MD by focusing on broad domains of behavioral function that can map onto underlying neural systems, namely deficits in hedonics, anticipatory behaviors, computations underlying value and effort, and effortful goal-directed behaviors needed to pursue rewarding outcomes. We highlight unique disturbances in each disorder that may involve dissociable neural systems, but also possible interactions between affect and cognition in MD versus SCZ. Finally, we review computational and translational approaches that offer mechanistic insight into how cellular-level disruptions can lead to complex affective disturbances, informing development of therapies across MD and SCZ.

Role of Serotonin in Punishment and Reward: New Vistas

The role of forebrain serotonin (or 5-hydroxytryptamine, 5-HT) in the chemical neuromodulation of mammalian behaviour remains unclear. Two prominent hypotheses are that it is implicated primarily in (i) behavioural inhibition; or ii) aversive punishment, although distinguishing between these hypotheses is difficult because of intrinsic asymmetries in how these systems control behavior. Previous, apparently paradoxical, findings appear to show that 5-HT depletion both reduces and enhances the effects of aversive reinforcers in humans and rodents, suggesting independent modulations of dissociable neural systems. Evidence will be surveyed from experimental animals, using intra-cerebral treatments with a selective 5-HT neurotoxin, 5,7 dihydroxytryptamine, or microinfusions of selective 5-HT receptor agents, and from human volunteers using acute dietary depletion of tryptophan (ATD) or systemic treatments with serotonin re-uptake inhibitors, in order to address these distinctions. Central manipulations of 5-HT generally disrupt behavioural inhibition, including both impulsive and compulsive behaviour, although often with no effect on sensitive measures of response inhibition in the stop-signal reaction time task. Some evidence in humans using ATD suggests that the behavioral inhibition is greater for aversively motivated than appetitively motivated behavior. However, in direct comparisons of effects of local depletions of 5-HT in the orbitofrontal cortex and amygdala in the marmoset monkey, both forms of motivated behavior are impaired, especially in the anticipatory phase of behavioural response to impending appetitive or aversive reinforcers. These findings are related to a variety of neuropsychiatric disorders in which 5-HT dysregulation has been postulated, including depression, drug addiction and obsessive-compulsive disorder.

Dissociable neural systems underwrite logical reasoning in the context of induced emotions with positive and negative valence.

How emotions influence syllogistic reasoning is not well understood. fMRI was employed to investigate the effects of induced positive or negative emotion on syllogistic reasoning. Specifically, on a trial-by-trial basis participants were exposed to a positive, negative, or neutral picture, immediately prior to engagement in a reasoning task. After viewing and rating the valence and intensity of each picture, participants indicated by keypress whether or not the conclusion of the syllogism followed logically from the premises. The content of all syllogisms was neutral, and the influence of belief-bias was controlled for in the study design. Emotion did not affect reasoning performance, although there was a trend in the expected direction based on accuracy rates for the positive (63%) and negative (64%) versus neutral (70%) condition. Nevertheless, exposure to positive and negative pictures led to dissociable patterns of neural activation during reasoning. Therefore, the neural basis of deductive reasoning differs as a function of the valence of the context.

Current Emotion Research in Cognitive Neuroscience: Linking Enhancing and Impairing Effects of Emotion on Cognition

Emotions can have both enhancing and impairing effects on various cognitive processes, from lower (e.g., perceptual) to higher level (e.g., mnemonic and executive) processes. The present article discusses emerging brain imaging evidence linking these opposing effects of emotion, which points to overlapping and dissociable neural systems involving both bottom-up and top-down mechanisms. The link between the enhancing and impairing effects is also discussed in a clinical context, with a focus on posttraumatic stress disorder (PTSD), where these opposing effects tend to co-occur, are exacerbated, and are detrimental. Overall, the present review highlights the need to consider together enhancing and impairing effects of emotion on cognition in studies investigating emotion–cognition interactions.