Resting state connectivity between medial temporal lobe regions and intrinsic cortical networks predicts performance in a path integration task

Humans differ in their individual navigational performance, in part because successful navigation relies on several diverse abilities. One such navigational capability is path integration, the updating of position and orientation during movement, typically in a sparse, landmark-free environment. This study examined the relationship between path integration abilities and functional connectivity to several canonical intrinsic brain networks. Intrinsic networks within the brain reflect past inputs and communication as well as structural architecture. Individual differences in intrinsic connectivity have been observed for common networks, suggesting that these networks can inform our understanding of individual spatial abilities. Here, we examined individual differences in intrinsic connectivity using resting state magnetic resonance imaging (rsMRI). We tested path integration ability using a loop closure task, in which participants viewed a single video of movement in a circle trajectory in a sparse environment, and then indicated whether the video ended in the same location in which it started. To examine intrinsic brain networks, participants underwent a resting state scan. We found that better performance in the loop task was associated with increased connectivity during rest between the central executive network (CEN) and posterior hippocampus, parahippocampal cortex (PHC) and entorhinal cortex. We also found that connectivity between PHC and the default mode network (DMN) during rest was associated with better loop closure performance. The results indicate that interactions between medial temporal lobe (MTL) regions and intrinsic networks that involve prefrontal cortex (PFC) are important for path integration and navigation.This work was supported by the Office of Naval Research (ONR MURI N00014-10-1-0936 and MURI N00014-16-1-2832). fMRI scanning was completed at the Athinoula A. Martinos Center for Biomedical Imaging (Charlestown, MA, USA), which receives support from the National Center for Research Resources (NCRR P41RR14075). (ONR MURI N00014-10-1-0936 - Office of Naval Research; MURI N00014-16-1-2832 - Office of Naval Research; NCRR P41RR14075 - National Center for Research Resources)Published versio

From Parallel Sequence Representations to Calligraphic Control: A Conspiracy of Neural Circuits

Calligraphic writing presents a rich set of challenges to the human movement control system. These challenges include: initial learning, and recall from memory, of prescribed stroke sequences; critical timing of stroke onsets and durations; fine control of grip and contact forces; and letter-form invariance under voluntary size scaling, which entails fine control of stroke direction and amplitude during recruitment and derecruitment of musculoskeletal degrees of freedom. Experimental and computational studies in behavioral neuroscience have made rapid progress toward explaining the learning, planning and contTOl exercised in tasks that share features with calligraphic writing and drawing. This article summarizes computational neuroscience models and related neurobiological data that reveal critical operations spanning from parallel sequence representations to fine force control. Part one addresses stroke sequencing. It treats competitive queuing (CQ) models of sequence representation, performance, learning, and recall. Part two addresses letter size scaling and motor equivalence. It treats cursive handwriting models together with models in which sensory-motor tmnsformations are performed by circuits that learn inverse differential kinematic mappings. Part three addresses fine-grained control of timing and transient forces, by treating circuit models that learn to solve inverse dynamics problems.National Institutes of Health (R01 DC02852

Hippocampal sclerosis affects fMR-adaptation of lyrics and melodies in songs

Songs constitute a natural combination of lyrics and melodies, but it is unclear whether and how these two song components are integrated during the emergence of a memory trace. Network theories of memory suggest a prominent role of the hippocampus, together with unimodal sensory areas, in the build-up of conjunctive representations. The present study tested the modulatory influence of the hippocampus on neural adaptation to songs in lateral temporal areas. Patients with unilateral hippocampal sclerosis and healthy matched controls were presented with blocks of short songs in which lyrics and/or melodies were varied or repeated in a crossed factorial design. Neural adaptation effects were taken as correlates of incidental emergent memory traces. We hypothesized that hippocampal lesions, particularly in the left hemisphere, would weaken adaptation effects, especially the integration of lyrics and melodies. Results revealed that lateral temporal lobe regions showed weaker adaptation to repeated lyrics as well as a reduced interaction of the adaptation effects for lyrics and melodies in patients with left hippocampal sclerosis. This suggests a deficient build-up of a sensory memory trace for lyrics and a reduced integration of lyrics with melodies, compared to healthy controls. Patients with right hippocampal sclerosis showed a similar profile of results although the effects did not reach significance in this population. We highlight the finding that the integrated representation of lyrics and melodies typically shown in healthy participants is likely tied to the integrity of the left medial temporal lobe. This novel finding provides the first neuroimaging evidence for the role of the hippocampus during repetitive exposure to lyrics and melodies and their integration into a song

Remembering Forward: Neural Correlates of Memory and Prediction in Human Motor Adaptation

We used functional MR imaging (FMRI), a robotic manipulandum and systems identification techniques to examine neural correlates of predictive compensation for spring-like loads during goal-directed wrist movements in neurologically-intact humans. Although load changed unpredictably from one trial to the next, subjects nevertheless used sensorimotor memories from recent movements to predict and compensate upcoming loads. Prediction enabled subjects to adapt performance so that the task was accomplished with minimum effort. Population analyses of functional images revealed a distributed, bilateral network of cortical and subcortical activity supporting predictive load compensation during visual target capture. Cortical regions – including prefrontal, parietal and hippocampal cortices – exhibited trial-by-trial fluctuations in BOLD signal consistent with the storage and recall of sensorimotor memories or “states” important for spatial working memory. Bilateral activations in associative regions of the striatum demonstrated temporal correlation with the magnitude of kinematic performance error (a signal that could drive reward-optimizing reinforcement learning and the prospective scaling of previously learned motor programs). BOLD signal correlations with load prediction were observed in the cerebellar cortex and red nuclei (consistent with the idea that these structures generate adaptive fusimotor signals facilitating cancelation of expected proprioceptive feedback, as required for conditional feedback adjustments to ongoing motor commands and feedback error learning). Analysis of single subject images revealed that predictive activity was at least as likely to be observed in more than one of these neural systems as in just one. We conclude therefore that motor adaptation is mediated by predictive compensations supported by multiple, distributed, cortical and subcortical structures

Adaptive Neural Models of Queuing and Timing in Fluent Action

Temporal structure in skilled, fluent action exists at several nested levels. At the largest scale considered here, short sequences of actions that are planned collectively in prefrontal cortex appear to be queued for performance by a cyclic competitive process that operates in concert with a parallel analog representation that implicitly specifies the relative priority of elements of the sequence. At an intermediate scale, single acts, like reaching to grasp, depend on coordinated scaling of the rates at which many muscles shorten or lengthen in parallel. To ensure success of acts such as catching an approaching ball, such parallel rate scaling, which appears to be one function of the basal ganglia, must be coupled to perceptual variables, such as time-to-contact. At a fine scale, within each act, desired rate scaling can be realized only if precisely timed muscle activations first accelerate and then decelerate the limbs, to ensure that muscle length changes do not under- or over-shoot the amounts needed for the precise acts. Each context of action may require a much different timed muscle activation pattern than similar contexts. Because context differences that require different treatment cannot be known in advance, a formidable adaptive engine-the cerebellum-is needed to amplify differences within, and continuosly search, a vast parallel signal flow, in order to discover contextual "leading indicators" of when to generate distinctive parallel patterns of analog signals. From some parts of the cerebellum, such signals controls muscles. But a recent model shows how the lateral cerebellum, such signals control muscles. But a recent model shows how the lateral cerebellum may serve the competitive queuing system (in frontal cortex) as a repository of quickly accessed long-term sequence memories. Thus different parts of the cerebellum may use the same adaptive engine system design to serve the lowest and the highest of the three levels of temporal structure treated. If so, no one-to-one mapping exists between levels of temporal structure and major parts of the brain. Finally, recent data cast doubt on network-delay models of cerebellar adaptive timing.National Institute of Mental Health (R01 DC02852

Brain networks for temporal adaptation, anticipation, and sensory-motor integration in rhythmic human behavior

Human interaction often requires the precise yet flexible interpersonal coordination of rhythmic behavior, as in group music making. The present fMRI study investigates the functional brain networks that may facilitate such behavior by enabling temporal adaptation (error correction), prediction, and the monitoring and integration of information about ‘self’ and the external environment. Participants were required to synchronize finger taps with computer-controlled auditory sequences that were presented either at a globally steady tempo with local adaptations to the participants' tap timing (Virtual Partner task) or with gradual tempo accelerations and decelerations but without adaptation (Tempo Change task). Connectome-based predictive modelling was used to examine patterns of brain functional connectivity related to individual differences in behavioral performance and parameter estimates from the adaptation and anticipation model (ADAM) of sensorimotor synchronization for these two tasks under conditions of varying cognitive load. Results revealed distinct but overlapping brain networks associated with ADAM-derived estimates of temporal adaptation, anticipation, and the integration of self-controlled and externally controlled processes across task conditions. The partial overlap between ADAM networks suggests common hub regions that modulate functional connectivity within and between the brain's resting-state networks and additional sensory-motor regions and subcortical structures in a manner reflecting coordination skill. Such network reconfiguration might facilitate sensorimotor synchronization by enabling shifts in focus on internal and external information, and, in social contexts requiring interpersonal coordination, variations in the degree of simultaneous integration and segregation of these information sources in internal models that support self, other, and joint action planning and prediction

Acute modulation of brain connectivity in Parkinson disease after automatic mechanical peripheral stimulation: A pilot study

The present study shows the results of a double-blind sham-controlled pilot trial to test whether measurable stimulus-specific functional connectivity changes exist after Automatic Mechanical Peripheral Stimulation (AMPS) in patients with idiopathic Parkinson Disease.Eleven patients (6 women and 5 men) with idiopathic Parkinson Disease underwent brain fMRI immediately before and after sham or effective AMPS. Resting state Functional Connectivity (RSFC) was assessed using the seed-ROI based analysis. Seed ROIs were positioned on basal ganglia, on primary sensory-motor cortices, on the supplementary motor areas and on the cerebellum. Individual differences for pre- and post-effective AMPS and pre- and post-sham condition were obtained and first entered in respective one-sample t-test analyses, to evaluate the mean effect of condition.Effective AMPS, but not sham stimulation, induced increase of RSFC of the sensory motor cortex, nucleus striatum and cerebellum. Secondly, individual differences for both conditions were entered into paired group t-test analysis to rule out sub-threshold effects of sham stimulation, which showed stronger connectivity of the striatum nucleus with the right lateral occipital cortex and the cuneal cortex (max Z score 3.12) and with the right anterior temporal lobe (max Z score 3.42) and of the cerebellum with the right lateral occipital cortex and the right cerebellar cortex (max Z score 3.79).Our results suggest that effective AMPS acutely increases RSFC of brain regions involved in visuo-spatial and sensory-motor integration.This study provides Class II evidence that automatic mechanical peripheral stimulation is effective in modulating brain functional connectivity of patients with Parkinson Disease at rest.Clinical Trials.gov NCT01815281