Introduction Use of functional MRI in awake non-human primate (NHPs) has recently increased. Scanning animals while awake makes data collection possible in the absence of anesthetic modulation and with an extended range of possible experimental designs. Robust awake NHP imaging however is challenging due to the strong artifacts caused by time-varying off-resonance changes introduced by the animal's body motion. In this study, we sought to thoroughly investigate the effect of a newly proposed dynamic off-resonance correction method on brain activation estimates using extended awake NHP data. Methods We correct for dynamic B0 changes in reconstruction of highly accelerated simultaneous multi-slice EPI acquisitions by estimating and correcting for dynamic field perturbations. Functional MRI data were collected in four male rhesus monkeys performing a decision-making task in the scanner, and analyses of improvements in sensitivity and reliability were performed compared to conventional image reconstruction. Results Applying the correction resulted in reduced bias and improved temporal stability in the reconstructed time-series data. We found increased sensitivity to functional activation at the individual and group levels, as well as improved reliability of statistical parameter estimates. Conclusions Our results show significant improvements in image fidelity using our proposed correction strategy, as well as greatly enhanced and more reliable activation estimates in GLM analyses.
Abstract Many psychiatric symptoms have been linked to threat-related perception and learning processes. In addition, however, there may also be mechanisms for balancing effectively between threat- and reward-related behaviors and these may also vary between individuals. We investigated neural activity associated with spontaneous switching between foraging for rewards and vigilance for threats with 7T fMRI. In a virtual naturalistic environment, participants freely switched between the two modes of behavior. Switching was driven by estimates of likelihood of threat and reward. Both tracking of threat and switching to vigilance were associated with specific but distributed patterns of activity spanning habenula, dorsal raphe nucleus (DRN), anterior cingulate cortex, and anterior insula cortex. Distinct distributed patterns heralded returns to reward-oriented behavior. Individual variation in DRN activity reflected individual variation in vigilance. All activity patterns were replicated in an initially held-out portion of data.
Decisions about when to act are critical for survival in humans as in animals, but how a desire is translated into the decision that an action is worth taking at any particular point in time is incompletely understood. Here we show that a simple model developed to explain when animals decide it is worth taking an action also explains a significant portion of the variance in timing observed when humans take voluntary actions. The model focuses on the current environment’s potential for reward, the timing of the individual’s own recent actions, and the outcomes of those actions. We show, by using ultrahigh-field MRI scanning, that in addition to anterior cingulate cortex within medial frontal cortex, a group of subcortical structures including striatum, substantia nigra, basal forebrain (BF), pedunculopontine nucleus (PPN), and habenula (HB) encode trial-by-trial variation in action time. Further analysis of the activity patterns found in each area together with psychophysiological interaction analysis and structural equation modeling suggested a model in which BF integrates contextual information that will influence the decision about when to act and communicates this information, in parallel with PPN and HB influences, to nigrostriatal circuits. It is then in the nigrostriatal circuit that action initiation per se begins.
ABSTRACT The dorsal raphe nucleus (DRN) is an important source of serotonin in the brain but fundamental aspects of its function remain elusive. Here, we present a combination of minimally invasive recording and disruption studies to show that DRN brings about changes in motivation states. We use recently developed methods for identifying temporal patterns in behaviour to show that monkeys change their motivation depending on the availability of rewards in the environment. Distinctive patterns of DRN activity occur when monkeys transition between a high motivation state occupied when rewards are abundant, to a low motivation state engendered by reward scarcity. Disrupting DRN diminishes sensitivity to the reward environment and perturbs transitions in motivational states.
Abstract The decision that it is worth doing something rather than nothing is a core yet understudied feature of voluntary behaviour. Here we study “willingness to act”, the probability of making a response given the context. Human volunteers encountered opportunities to make effortful actions in order to receive rewards, while watching a movie inside a 7 T MRI scanner. Reward and other context features determined willingness-to-act. Activity in the habenula tracked trial-by-trial variation in participants’ willingness-to-act. The anterior insula encoded individual environment features that determined this willingness. We identify a multi-layered network in which contextual information is encoded in the anterior insula, converges on the habenula, and is then transmitted to the supplementary motor area, where the decision is made to either act or refrain from acting via the nigrostriatal pathway.
Abstract Use of functional MRI in awake non-human primate (NHPs) has recently increased. Scanning animals while awake makes data collection possible in the absence of anaesthetic modulation and with an extended range of possible experimental designs. Robust awake NHP imaging however is challenging due to the strong artifacts caused by time-varying off-resonance changes introduced by the animal’s body motion. Recently, an image reconstruction technique has been proposed to estimate these off-resonance changes using the navigator data that is typically collected during fMRI scans to correct the data and compensate for the changes. In this study, we sought to thoroughly investigate the effect of this correction on the brain activation estimates using extended awake NHP data. Our results show significant improvements in image fidelity using our proposed correction strategy, as well as greatly enhanced and more reliable activation estimates in GLM analyses.
Daily life for humans and other animals requires switching between periods of threat- and reward-oriented behavior. We investigated neural activity associated with spontaneous switching, in a naturalistic task, between foraging for rewards and seeking information about potential threats with 7T fMRI in healthy humans. Switching was driven by estimates of likelihood of threat and reward. Both tracking of threat and switching to a vigilant mode in which people sought more information about potential threats were associated with specific but distributed patterns of activity spanning habenula, dorsal raphe nucleus (DRN), anterior cingulate cortex, and anterior insula cortex. Different aspects of the distributed activity patterns were linked to monitoring the threat level, seeking information about the threat, and actual threat detection. A distinct pattern of activity in the same circuit and elsewhere occurred during returns to reward-oriented behavior. Individual variation in DRN activity reflected individual variation in the seeking of information about threats.
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