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Lapate, R. C.

Publications and source records attributed to Lapate, R. C..

12 recordsLinked to original sources

Neural Control of Autonomic Arousal During Threat Anticipation Revealed by High-Resolution Cardiac Contractility

The sympathetic nervous system prepares the organism for adaptive action by shaping physiological, affective, and behavioral responses to environmental demands. Yet, how sympathetic signals dynamically couple with neural systems supporting emotional experience and behavior remains poorly understood, in part because common indices such as skin conductance responses lack sufficient temporal resolution to track these dynamics. Here, we evaluated trans-radial electrical bioimpedance velocimetry (TREV), a non-invasive measure of beat-to-beat cardiac contractility, and compared it with skin conductance responses during threat anticipation and simultaneous fMRI. Participants (n=60) completed a threat-of-shock paradigm requiring goal-directed action. Cardiac contractility increased during threat anticipation, covaried with skin conductance responses, and independently predicted self-reported emotional intensity. Critically, threat-related increases in contractility--but not skin conductance--tracked threat-related modulation of activation in dorsomedial prefrontal cortex, posterior parietal cortex, and cerebellum, with contractility-modulated cerebellar activation predicting faster motor responses under threat. These findings establish TREV-derived cardiac contractility as a physiological signal linking sympathetic drive with neural responding, emotional experience, and adaptive behavioral mobilization during emotion-guided action.

neuroscience↗

Distinct amygdalar pathways to frontopolar cortex and medial temporal lobe support temporal memory for emotional events

Growing evidence suggests that emotion shapes temporal aspects of memory--such as remembering when an event occurred--yet the neural bases of these effects remain unclear. Prior work indicates that temporal-context representations in memory are supported by the function of medial temporal lobe (MTL) and prefrontal regions with privileged access to amygdala-originated affective signals, which may mediate emotional influences on temporal memory--including hippocampus, perirhinal cortex, and lateral frontopolar cortex (FPl). To test whether these candidate pathways shape temporal memory for emotional events, participants encoded trial-unique negative and positive images in the scanner, followed by a surprise temporal memory task. We found that more negative stimuli were associated with greater amygdala activation and lower temporal-memory error for when emotional images occurred. Replicating and extending prior work, higher stimulus-evoked multivoxel pattern similarity in the hippocampus (between trials) and FPl (within and between trials) was associated with higher temporal memory errors. Notably, greater amygdala responding to emotional images predicted higher between-trial pattern similarity in the hippocampus, but lower within- and between-trial similarity in FPl. Amygdala engagement was also correlated with greater perirhinal activation, which in turn predicted stronger item memory and a recency bias in temporal memory estimates. Collectively, these findings reveal distinct--and opposing--modulatory effects of amygdala-FPl and amygdala-MTL pathways on temporal memory, with the potential to sharpen and blur memory for when emotional events occurred. Significance statementEmotional events influence how we remember time. Prior work implicates function of the lateral frontal pole (FPl) and medial temporal lobe (MTL) regions--including hippocampus and perirhinal cortex--in temporal memory. Yet, whether and how these areas support temporal memory for emotional events remains unclear. Using trial-unique emotional images, we found that negative-emotional valence was associated with stronger amygdala activation and temporal-memory accuracy. Higher pattern similarity in hippocampus and FPl predicted worse temporal memory. Notably, amygdala activation predicted higher between-trial hippocampal pattern similarity but lower within-trial FPl similarity. Perirhinal engagement, which correlated with amygdala activation and item memory, predicted a recency bias in temporal-memory judgments. Together, these findings reveal distinct amygdala-MTL and amygdala-prefrontal pathways through which emotion shapes temporal memory.

neuroscience↗

Cardiac-sympathetic state predicts action restraint, gated by demonstrated agency

Withholding action until the appropriate moment is a core challenge of motivated behavior. Using beat-to-beat cardiac contractility during an incentivized reaching task, we show that cardiac-sympathetic outflow predicts action restraint. Under high-reward conditions that induce a speed-accuracy tradeoff, reduced contractility at the time of instruction preceded premature responses (false starts). Under high-loss-avoidance conditions, elevated pre-movement contractility predicted slower, more controlled initiation, but only among participants with above-median task success. These findings suggest cardiac-sympathetic engagement does not simply serve mobilization but flexibly supports context-appropriate action regulation, with recruitment for restraint gated by demonstrated agency.

physiology↗

Incentive valence differentially engages open- and closed-loop basal ganglia circuits during movement initiation

Incentives modulate voluntary movement, yet the circuitry channeling these signals into motor output remains unclear. Classical models emphasize a closed-loop circuit (CLC) linking dorsal putamen (PUTd) with motor cortex, but this pathway is anatomically segregated from affective processing regions. Anatomical and clinical evidence point to an alternative: an open-loop circuit (OLC) from ventral putamen (PUTv) that may route affective signals to motor cortex. Here, we conducted two experiments to test whether a functional OLC exists in humans and whether it is differentially engaged by incentive conditions. First, in 7 T resting-state fMRI (multi-echo), PUTv showed robust functional connectivity with both affective and motor regions, including the cingulate motor area (CMA), even after accounting for PUTd variance. This connectivity pattern supports the plausibility of an independent pathway linking affective basal ganglia regions to the motor cortex. Second, in 3 T task fMRI (incentivized reaching), jackpot (high-reward) and robber (high-loss avoidance) incentive conditions produced distinct behavioral and neural signatures. Jackpot produced a speed-accuracy trade-off, with faster movement initiation but more false starts. Neurally, this coincided with engagement (BOLD responses relevant for initiation speed) being reduced in CLC nodes but not in OLC. Robber, in contrast, eliminated engagement in both OLC and CLC nodes, instead recruiting stopping-related regions (e.g., STN), consistent with an avoidance phenomenology. Together, these findings support a versatile architecture for movement initiation that flexibly engages distinct cortico-subcortical circuits depending on incentive phenomenology, and offer a candidate mechanism through which affective salience and valence modulate voluntary movement. Significance StatementAffective signals profoundly influence movement, yet the mechanisms linking motivationally relevant contexts with motor behavior remain unclear. Combining ultra-high field (7 T) connectomics with task-based (3 T) neuroimaging, we provide the first systems-level evidence in humans for such a mechanism: a ventral putamen-centered open-loop circuit (OLC) connecting affective and motor areas, operating alongside the canonical dorsal putamen-centered closed-loop sensorimotor circuit (CLC). Critically, the phenomenological quality of incentive (how it is construed as reward versus threat) rather than magnitude alone, likely determines which circuit dominates during movement initiation. These findings help to explain paradoxical kinesia in Parkinsons disease, where affective contexts can bypass degraded sensorimotor circuits, and establish foundations for context-based therapeutic interventions.

neuroscience↗

Integrated Representations of Threat and Controllability in the Lateral Frontal Pole

Emotional processing is ubiquitous in everyday life, informing goal pursuit not only in response to current demands, but also in anticipation of future outcomes. Lateral prefrontal (LPFC) function supports cognitive control, and emerging evidence suggests a unique role for its anterior-most region--the lateral frontal pole (FPl)--in integrating putatively amygdala-originated emotion signals with goal information. However, whether these organizational properties of LPFC are expressed during the anticipation of future threat remains unknown. Here, we used FIR modeling and pattern similarity analysis to examine dynamic engagement and representational properties of distinct LPFC regions during threat anticipation requiring goal-directed action. Healthy participants (n=67) were scanned during a threat-of-shock paradigm consisting of a prolonged (18s) countdown to possible shock administration. Threat unpleasantness and controllability were manipulated orthogonally: in controllable trials, participants could avoid an unpleasant or mild shock by making a successful time-sensitive response; in uncontrollable trials, shocks were administered regardless of performance. LPFC robustly coded for anticipated threat unpleasantness, with FPl showing the strongest modulation by threat unpleasantness and controllability relative to caudal and mid-LPFC regions. Caudal and mid-LPFC maintained independent representations of threat unpleasantness and controllability. In contrast, FPl held conjunctive threat-and-controllability representations, which were associated with successful motor performance following anticipation of unpleasant shocks. Stronger conjunctive FPl representations were also associated with greater inverse amygdala-FPl coupling. Together, these findings provide insight into LPFC organization under naturalistic emotional challenges and highlight a key role for FPl in integrating affective and control-related information during threat anticipation to support goal-directed action. Significance StatementAnticipating emotionally-charged events--such as a painful outcome we may or may not be able to avoid--requires integrating emotion and control to guide behavior. However, the neural mechanisms through which emotional states influence goal-directed behavior in naturalistic, anticipatory emotional contexts remain unclear. Using a threat-of-shock paradigm and multivariate analyses we show that the anterior-most region of the lateral prefrontal cortex (LPFC)--the lateral frontal pole (FPl)--uniquely integrates information about the emotional unpleasantness and controllability of a future event, and that the strength of this integrated signal predicts better behavioral performance. These findings extend models of LPFC function to naturalistic, emotional contexts, and highlight the FPl as a key node for translating emotional and behavioral-control information into adaptive action.

neuroscience↗

Dissociation of putative open loop circuit from ventral putamen to motor cortical areas in humans I: high-resolution connectomics

Human movement is partly organized and executed by cortico-basal ganglia-thalamic closed-loop circuits (CLCs), wherein motor cortical areas both send inputs to and receive feedback from the basal ganglia, particularly the dorsal putamen (PUTd). These networks are compromised in Parkinsons disease (PD) due to neurodegeneration of dopaminergic inputs primarily to PUTd. Yet, fluid movement in PD can sporadically occur, especially when induced by emotionally arousing events. Rabies virus tracing in non-human primates has identified a potential alternative motor pathway, wherein the ventral putamen (PUTv) receives inputs from subcortical limbic areas (such as amygdala nuclei) and sends outputs to motor cortical areas putatively via the nucleus basalis of Meynert (NBM). We hypothesize that this separable open loop circuit (OLC) may exist in humans and explain the preservation of movement after CLC degradation. Here, we provide evidence for the normal human OLC with ultra-high field (7T), multi-echo functional magnetic resonance imaging. We acquired resting-state functional connectivity (FC) scans from 21 healthy adults (avg. age = 29, 12M/9F, all right-handed) and mapped left-hemisphere seed-to-voxel connectivity to assess PUTv FC with putative subcortical nodes and motor cortical areas. We found that putative OLC node (basolateral amygdala, NBM) FC was greater with PUTv (p < 0.05), while CLC subcortical seed (ventrolateral nucleus of thalamus) FC was greater with PUTd (p<0.01). Striatal FC patterns varied across cortical motor areas, with cingulate (p < 0.0001) and supplementary (p < 0.0001) motor areas showing greater FC with PUTv vs. nucleus accumbens. SMA had greater FC with PUTd vs. PUTv (p < 0.0001), while cingulate and primary motor areas showed no significant differences in FC between PUTd and PUTv (p > 0.1). Collectively, these results suggest that PUTv is functionally connected to motor cortical areas and may be integrated into a separable motor OLC with subcortical limbic inputs.

neuroscience↗

Dissociation of novel open loop from ventral putamen to motor areas from classic closed loop in humans II: task-based function

Humans ubiquitously increase the speed of their movements when motivated by incentives (i.e., capturing reward or avoiding loss). The complex interplay between incentivization and motor output is pertinent for unpacking the functional profiles of different circuits that link the basal ganglia with motor cortical areas. Here, we analyzed the functional profile of nodes forming two circuits involving putamen and motor cortical areas: the traditional "closed-loop circuit" (CLC) from sensorimotor dorsal putamen (PUTd) and a putative "open-loop circuit" (OLC) from ventral putamen (PUTv). Establishing differential function between CLC and OLC is particularly relevant for therapeutic approaches to Parkinsons disease, where OLC function is hypothesized to be relatively spared by the disease process. In a large sample fMRI study, 68 healthy controls executed speeded reaches with a joystick under different levels of incentivization to accurately hit precision targets. We dissociated effects of "incentive per se" (i.e., changes in brain activity when an upcoming movement obtains a reward or avoids a loss) from "RT effects" (i.e., brain activity that directly scales with adjustments to movement initiation time). Incentive per se was observed across sites in both CLC and OLC. However, RT effects were primarily in nodes of the OLC and motor sites, consistent with the hypothesized anatomy and function of OLC. Our findings additionally suggest valence might mediate when incentives recruit OLC to more prominent control of motor behavior.

neuroscience↗

Emotional state dynamics impacts temporal memory

Emotional fluctuations are ubiquitous in everyday life, but precisely how they sculpt the temporal organization of memories remains unclear. Here, we designed a novel task--the Emotion Boundary Task--wherein participants viewed sequences of negative and neutral images surrounded by a color border. We manipulated perceptual context (border color), emotional valence, as well as the direction of emotional-valence shifts (i.e., shifts from neutral-to-negative and negative-to-neutral events) to create encoding events comprised of image sequences with a shared perceptual and/or emotional context. We measured memory for temporal order and subjectively remembered temporal distances for images processed within and across events. Negative images processed within events were remembered as closer in time compared to neutral ones. In contrast, temporal distance was remembered as longer for images spanning neutral-to-negative shifts-- suggesting temporal dilation in memory with the onset of a negative event following a previously-neutral state. The extent of this negative-picture induced temporal dilation in memory correlated with dispositional negativity across individuals. Lastly, temporal order memory was enhanced for recently presented negative (compared to neutral) images. These findings suggest that emotional-state dynamics matters when considering emotion-temporal memory interactions: While persistent negative events may compress subjectively remembered time, dynamic shifts from neutral to negative events produce temporal dilation in memory, which may be relevant for adaptive emotional functioning.

animal behavior and cognition↗

Long-term meditation training is associated with enhanced attention and stronger posterior cingulate - rostrolateral prefrontal cortex resting connectivity

Mindfulness meditation has been shown to increase resting state functional connectivity (rsFC) between the posterior cingulate cortex (PCC) and dorsolateral prefrontal cortex (DLPFC), which is thought to reflect improvements in attention to the present moment. However, prior research in long-term meditation practitioners lacked quantitative measures of attention that would provide a more direct behavioral correlate and interpretational anchor for PCC-DLPFC connectivity and was inherently limited by small sample sizes. Moreover, whether mindfulness meditation primarily impacts brain function locally, or impacts the dynamics of large-scale brain networks, remained unclear. Here, we sought to replicate and extend prior findings of increased PCC - DLPFC rsFC in a sample of 40 long-term meditators (average practice= 3759 hours) who also completed a behavioral assay of attention. In addition, we tested a network-based framework of changes in inter-regional connectivity by examining network-level connectivity. We found that meditators had stronger PCC-rostrolateral prefrontal cortex (PFC) rsFC, lower connector hub strength across the default mode network (DMN) relative to other functional networks, and better attention to task, compared to 124 meditation-naive controls. Orienting attention positively correlated with PCC- rostrolateral PFC connectivity, and negatively correlated with DMN connector hub strength. These findings provide novel evidence that posterior cingulate - rostrolateral PFC rsFC may support attention orienting, consistent with a role for rostrolateral PFC in meta-cognitive background awareness that is a core component of mindfulness meditation training. Our results further demonstrate that long-term mindfulness meditation may improve attention and strengthen the underlying brain networks.

neuroscience↗

Emotional context sculpts action goal representations in the lateral frontal pole

Emotional states provide an ever-present source of contextual information that should inform behavioral goals. Despite the ubiquity of emotional signals in our environment, the neural mechanisms underlying their influence on goal-directed action remains unclear. Prior work suggests that the lateral frontal pole (FPl) is uniquely positioned to integrate affective information into cognitive control representations. We used pattern similarity analysis to examine the content of representations in FPl and interconnected mid-lateral prefrontal and amygdala circuitry. Healthy participants (n=37; n=21 females) were scanned while undergoing an event-related Affective Go/No-Go task, which requires goal-oriented action selection during emotional processing. We found that FPl contained conjunctive emotion-action goal representations that were related to successful cognitive control during emotional processing. These representations differed from conjunctive emotion-action goal representations found in the basolateral amygdala. While robust action goal representations were present in mid-lateral prefrontal cortex, they were not modulated by emotional valence. Finally, converging results from functional connectivity and multivoxel pattern analyses indicated that FPls emotional valence signals likely originated from interconnected subgenual ACC (BA25), which was in turn functionally coupled with the amygdala. Thus, our results identify a key pathway by which internal emotional states influence goal-directed behavior. Significance statementOptimal functioning in everyday life requires behavioral regulation that flexibly adapts to dynamically changing emotional states. However, precisely how emotional states influence goal-directed action remains unclear. Unveiling the neural architecture that supports emotion-goal integration is critical for our understanding of disorders such as psychopathy, which is characterized by deficits in incorporating emotional cues into goals, as well as mood and anxiety disorders, which are characterized by impaired goal-based emotion regulation. Our study identifies a key circuit through which emotional states influence goal-directed behavior. This circuitry comprised the lateral frontal pole (FPl), which represented integrated emotion-goal information, as well as interconnected amygdala and subgenual ACC, which conveyed emotional signals to FPl.

neuroscience↗

Perceptual metacognition of human faces is causally supported by function of the lateral prefrontal cortex

Metacognitive visual awareness--the ability to know that one is having a particular visual experience--is thought to optimally guide behavior and help us accurately navigate our complex social environments. Yet the neural underpinnings of visual metacognition continue to be the subject of vigorous debate: While prior work identified correlations between perceptual metacognitive ability and the structure and function of lateral prefrontal cortex (LPFC), evidence for a causal role of this region in promoting metacognition is controversial--in fact, some question whether the prefrontal cortex plays any role in supporting conscious visual experiences. Moreover, whether LPFC function promotes metacognitive awareness of perceptual and emotional features of complex, yet ubiquitous socio-emotional face stimuli is unknown. Using model-based analyses following a causal intervention to LPFC in humans, we demonstrate that LPFC promotes metacognitive awareness of the orientation of emotional faces--although not of their emotional expressions. Effects were specific to metacognition, as LPFC perturbation did not alter stimulus discrimination performance. Collectively, these data support the causal involvement of the prefrontal cortex in metacognitive awareness, and indicate that the role of LPFC function in metacognition encompasses perceptual experiences of naturalistic social stimuli.

neuroscience↗

Behavioral and neural indices of affective coloring for neutral social stimuli

Emotional processing often continues beyond the presentation of emotionally evocative stimuli, which can result in affective biasing or coloring of subsequently encountered events. Here, we describe neural correlates of affective coloring and examine how individual differences in affective style impact the magnitude of affective coloring. We conducted functional magnetic resonance imaging in 117 adults who passively viewed negative, neutral, and positive pictures presented 2s prior to neutral faces. Brain responses to neutral faces were modulated by the valence of preceding pictures, with greater activation for faces following negative (vs. positive) pictures in the amygdala, dorsomedial and lateral prefrontal cortex, ventral visual cortices, posterior superior temporal sulcus, and angular gyrus. Three days after the MRI scan, participants rated their memory and liking of previously encountered neutral faces. Individuals higher in trait positive affect and emotional reappraisal rated faces as more likable when preceded by emotionally arousing (negative or positive) pictures. Additionally, greater amygdala responses to neutral faces preceded by positively valenced pictures were associated with greater memory for these faces three days later. Collectively, these results reveal individual differences in how emotions spill over onto the processing of unrelated social stimuli, resulting in persistent and affectively biased evaluations of such stimuli.

neuroscience↗