Elena Beanato, Hyuk-June Moon, Fabienne Windel, Pierre Vassiliadis, Maximillian J. Wessel, Traian Popa, Menoud Pauline, Esra Neufeld, Emanuela De Falco, Baptiste Gauthier, Melanie Steiner, Olaf Blanke, Friedhelm C. Hummel <<<

Because of the depth of the hippocampal-entorhinal complex (HC-EC) in the brain, understanding of its role in spatial navigation via neuromodulation was limited in humans. Here, we aimed to better elucidate this relationship in healthy volunteers, using transcranial temporal interference electric stimulation (tTIS), a noninvasive technique allowing to selectively neuromodulate deep brain structures. We applied tTIS to the right HC-EC in either continuous or intermittent theta-burst stimulation patterns (cTBS or iTBS), compared to a control condition, during a virtual reality–based spatial navigation task and concomitant functional magnetic resonance imaging. iTBS improved spatial navigation performance, correlated with hippocampal activity modulation, and decreased grid cell–like activity in EC. Collectively, these data provide the evidence that human HC-EC activity can be directly and noninvasively modulated leading to changes of spatial navigation behavior. These findings suggest promising perspectives for patients suffering from cognitive impairment such as following traumatic brain injury or dementia. <<<

The hippocampus and entorhinal cortex have been linked to both memory functions and to spatial cognition, but it has been unclear how these ideas relate to each other. An important part of spatial cognition is the ability to keep track of a reference location using self-motion cues (sometimes referred to as path integration), and it has been suggested that the hippocampus or entorhinal cortex is essential for this ability. Patients with hippocampal lesions or larger lesions that also included entorhinal cortex were led on paths while blindfolded (up to 15 m in length) and were asked to actively maintain the path in mind. Patients pointed to and estimated their distance from the start location as accurately as controls. A rotation condition confirmed that performance was based on self-motion cues. When demands on long-term memory were increased, patients were impaired. Thus, in humans, the hippocampus and entorhinal cortex are not essential for path integration. <<<

We reliably judge locations of static objects when we walk despite the retinal images of these objects moving with every step we take. Here, we showed our brains solve this optical illusion by adopting an allocentric spatial reference frame. We measured perceived target location after the observer walked a short distance from the home base. Supporting the allocentric coding scheme, we found the intrinsic bias , which acts as a spatial reference frame for perceiving location of a dimly lit target in the dark, remained grounded at the home base rather than traveled along with the observer. The path-integration mechanism responsible for this can utilize both active and passive (vestibular) translational motion signals, but only along the horizontal direction. This asymmetric path-integration finding in human visual space perception is reminiscent of the asymmetric spatial memory finding in desert ants, pointing to nature’s wondrous and logically simple design for terrestrial creatures. <<<

Terrains in a 3D world can be undulating. Yet, most prior research has exclusively investigated spatial representations on a flat surface, leaving a 2D cognitive map as the dominant model in the field. Here, we investigated whether humans represent a curved surface by building a dimension-reduced flattened 2D map or a full 3D map. Participants learned the location of objects positioned on a flat and curved surface in a virtual environment by driving on the concave side of the surface (Experiment 1), driving and looking vertically (Experiment 2), or flying (Experiment 3). Subsequently, they were asked to retrieve either the path distance or the 3D Euclidean distance between the objects. Path distance estimation was good overall, but we found a significant underestimation bias for the path distance on the curve, suggesting an influence of potential 3D shortcuts, even though participants were only driving on the surface. Euclidean distance estimation was better when participants were exposed more to the global 3D structure of the environment by looking and flying. These results suggest that the representation of the 2D manifold, embedded in a 3D world, is neither purely 2D nor 3D. Rather, it is flexible and dependent on the behavioral experience and demand. <<<

Path integration, the ability to sense self-motion for keeping track of changes in orientation and position, constitutes a fundamental mechanism of spatial navigation and a keystone for the development of cognitive maps. Whereas animal path integration is predominantly supported by the head-direction, grid, and place cell systems, the neural foundations are not well understood in humans. Here we used functional magnetic resonance imaging and a virtual rendition of a triangle completion paradigm to test whether human path integration recruits a cortical system similar to that of rodents and nonhuman primates. Participants traveled along two legs of a triangle before pointing toward the starting location. In accordance with animal models, stronger right hippocampal activation predicted more accurate updating of the starting location on a trial-by-trial basis. Moreover, between-subjects fluctuations in response consistency were negatively correlated with bilateral hippocampal and medial prefrontal activation, and bilateral recruitment of the human motion complex (hMT+) covaried with individual path integration capability. Given that these effects were absent in a perceptual control task, the present study provides the first evidence that visual path integration is related to the dynamic interplay of self-motion processing in hMT+, higher-level spatial processes in the hippocampus, and spatial working memory in medial prefrontal cortex. <<<

The hippocampal formation contains neurons responsive to an animal's current location and orientation, which together provide the organism with a neural map of space. Spatially tuned neurons rely on external landmark cues and internally generated movement information to estimate position. An important class of landmark cue are the boundaries delimiting an environment, which can define place cell field position and stabilize grid cell firing. However, the precise nature of the sensory information used to detect boundaries remains unknown. We used 2-dimensional virtual reality (VR) to show that visual cues from elevated walls surrounding the environment are both sufficient and necessary to stabilize place and grid cell responses in VR, when only visual and self-motion cues are available. By contrast, flat boundaries formed by the edges of a textured floor did not stabilize place and grid cells, indicating only specific forms of visual boundary stabilize hippocampal spatial firing. Unstable grid cells retain internally coherent, hexagonally arranged firing fields, but these fields "drift" with respect to the virtual environment over periods >5 s. Optic flow from a virtual floor does not slow drift dynamics, emphasizing the importance of boundary-related visual information. Surprisingly, place fields are more stable close to boundaries even with floor and wall cues removed, suggesting invisible boundaries are inferred using the motion of a discrete, separate cue (a beacon signaling reward location). Subsets of place cells show allocentric directional tuning toward the beacon, with strength of tuning correlating with place field stability when boundaries are removed. <<<

When observers have prior knowledge about the likely outcome of their perceptual decisions, they exhibit robust behavioural biases in reaction time and choice accuracy. Computational modelling typically attributes these effects to strategic adjustments in the criterion amount of evidence required to commit to a choice alternative - usually implemented by a starting point shift - but recent work suggests that expectations may also fundamentally bias the encoding of the sensory evidence itself. Here, we recorded neural activity with EEG while participants performed a contrast discrimination task with valid, invalid, or neutral probabilistic cues across multiple testing sessions. We measured sensory evidence encoding via contrast-dependent steady-state visual-evoked potentials (SSVEP), while a read-out of criterion adjustments was provided by effector-selective mu-beta band activity over motor cortex. In keeping with prior modelling and neural recording studies, cues evoked substantial biases in motor preparation consistent with criterion adjustments, but we additionally found that the cues produced a significant modulation of the SSVEP during evidence presentation. While motor preparation adjustments were observed in the earliest trials, the sensory-level effects only emerged with extended task exposure. Our results suggest that, in addition to strategic adjustments to the decision process, probabilistic information can also induce subtle biases in the encoding of the evidence itself. <<<

The hippocampal-entorhinal system encodes a map of space that guides spatial navigation. Goal-directed behaviour outside of spatial navigation similarly requires a representation of abstract forms of relational knowledge. This information relies on the same neural system, but it is not known whether the organisational principles governing continuous maps may extend to the implicit encoding of discrete, non-spatial graphs. Here, we show that the human hippocampal-entorhinal system can represent relationships between objects using a metric that depends on associative strength. We reconstruct a map-like knowledge structure directly from a hippocampal-entorhinal functional magnetic resonance imaging adaptation signal in a situation where relationships are non-spatial rather than spatial, discrete rather than continuous, and unavailable to conscious awareness. Notably, the measure that best predicted a behavioural signature of implicit knowledge and blood oxygen level-dependent adaptation was a weighted sum of future states, akin to the successor representation that has been proposed to account for place and grid-cell firing patterns. <<<

Temporal binding has been understood as an illusion in timing judgment. When an action triggers an outcome (e.g. a sound) after a brief delay, the action is reported to occur later than if the outcome does not occur, and the outcome is reported to occur earlier than a similar outcome not caused by an action. We show here that an attention mechanism underlies the seeming illusion of timing judgment. In one method, participants watch a rotating clock hand and report event times by noting the clock hand position when the event occurs. We find that visual spatial attention is critically involved in shaping event time reports made in this way. This occurs because action and outcome events result in shifts of attention around the clock rim, thereby biasing the perceived location of the clock hand. Using a probe detection task to measure attention, we show a difference in the distribution of visual spatial attention between a single-event condition (sound only or action only) and a two-event agency condition (action plus sound). Participants accordingly report the timing of the same event (the sound or the action) differently in the two conditions: spatial attentional shifts masquerading as temporal binding. Furthermore, computational modeling based on the attention measure can reproduce the temporal binding effect. Studies that use time judgment as an implicit marker of voluntary agency should first discount the artefactual changes in event timing reports that actually reflect differences in spatial attention. The study also has important implications for related results in mental chronometry obtained with the clock-like method since Wundt, as attention may well be a critical confounding factor in the interpretation of these studies. <<<

Human perceptual decisions can be repelled away from (repulsive adaptation) or attracted towards recent visual experience (attractive serial dependence). It is currently unclear whether and how these repulsive and attractive biases interact during visual processing and what computational principles underlie these history dependencies. Here we disentangle repulsive and attractive biases by exploring their respective timescales. We find that perceptual decisions are concurrently attracted towards the short-term perceptual history and repelled from stimuli experienced up to minutes into the past. The temporal pattern of short-term attraction and long-term repulsion cannot be captured by an ideal Bayesian observer model alone. Instead, it is well captured by an ideal observer model with efficient encoding and Bayesian decoding of visual information in a slowly changing environment. Concurrent attractive and repulsive history biases in perceptual decisions may thus be the consequence of the need for visual processing to simultaneously satisfy constraints of efficiency and stability. <<<

Our ability to enact successful goal-directed actions involves multiple learning processes. Among these processes, implicit motor adaptation ensures that the sensorimotor system remains finely tuned in response to changes in the body and environment. Whether Parkinson's disease impacts implicit motor adaptation remains a contentious area of research: whereas multiple reports show impaired performance in this population, many others show intact performance. While there is a range of methodological differences across studies, one critical issue is that performance in many of the studies may reflect a combination of implicit adaptation and strategic re-aiming. Here, we revisited this controversy using a visuomotor task designed to isolate implicit adaptation. In two experiments, we found that adaptation in response to a wide range of visual perturbations was similar in Parkinson's disease and matched control participants. Moreover, in a meta-analysis of previously published and unpublished work, we found that the mean effect size contrasting Parkinson's disease and controls across 16 experiments involving over 200 participants was not significant. Together, these analyses indicate that implicit adaptation is preserved in Parkinson's disease, offering a fresh perspective on the role of the basal ganglia in sensorimotor learning. <<<

AbstractPerceptual decisions should depend on sensory evidence. However, such decisions are also influenced by past choices and outcomes. These choice history biases may reflect advantageous strategies to exploit temporal regularities of natural environments. However, it is unclear whether and how observers can adapt their choice history biases to different temporal regularities, to exploit the multitude of temporal correlations that exist in nature. Here, we show that mice adapt their perceptual choice history biases to different temporal regularities. This adaptation is well captured by a normative reinforcement learning algorithm with multi-trial belief states, comprising both current trial sensory and previous trial memory states. We demonstrate that striatal dopamine tracks predictions of the model and behavior, pointing towards the involvement of dopamine in forming adaptive history biases. Our results reveal the adaptive nature of perceptual choice history biases, and shed light on their underlying computational principles and neural implementation. <<<

Reinforcement learning (RL) models have been influential in characterizing human learning and decision making, but few studies apply them to characterizing human spatial navigation and even fewer systematically compare RL models under different navigation requirements. Because RL can characterize one's learning strategies quantitatively and in a continuous manner, and one's consistency of using such strategies, it can provide a novel and important perspective for understanding the marked individual differences in human navigation and disentangle navigation strategies from navigation performance. One-hundred and fourteen participants completed wayfinding tasks in a virtual environment where different phases manipulated navigation requirements. We compared performance of five RL models (3 model-free, 1 model-based and 1 "hybrid") at fitting navigation behaviors in different phases. Supporting implications from prior literature, the hybrid model provided the best fit regardless of navigation requirements, suggesting the majority of participants rely on a blend of model-free (route-following) and model-based (cognitive mapping) learning in such navigation scenarios. Furthermore, consistent with a key prediction, there was a correlation in the hybrid model between the weight on model-based learning (i.e., navigation strategy) and the navigator's exploration vs. exploitation tendency (i.e., consistency of using such navigation strategy), which was modulated by navigation task requirements. Together, we not only show how computational findings from RL align with the spatial navigation literature, but also reveal how the relationship between navigation strategy and a person's consistency using such strategies changes as navigation requirements change. <<<

We share data from N = 217 healthy adults (mean age 29 years, range 20-41; 109 females, 108 males) who underwent extensive cognitive assessment and neuroimaging to examine the neural basis of individual differences, with a particular focus on a brain structure called the hippocampus. Cognitive data were collected using a wide array of questionnaires, naturalistic tests that examined imagination, autobiographical memory recall and spatial navigation, traditional laboratory-based tests such as recalling word pairs, and comprehensive characterisation of the strategies used to perform the cognitive tests. 3 Tesla MRI data were also acquired and include multi-parameter mapping to examine tissue microstructure, diffusion-weighted MRI, T2-weighted high-resolution partial volume structural MRI scans (with the masks of hippocampal subfields manually segmented from these scans), whole brain resting state functional MRI scans and partial volume high resolution resting state functional MRI scans. This rich dataset will be of value to cognitive and clinical neuroscientists researching individual differences, real-world cognition, brain-behaviour associations, hippocampal subfields and more. All data are freely available on Dryad. <<<

Hemispheric specialization is a fundamental feature of human brain organization. However, it is not yet clear to what extent the lateralization of specific cognitive processes may be evident throughout the broad functional architecture of cortex. While the majority of people exhibit left-hemispheric language dominance, a substantial minority of the population shows reverse lateralization. Using twin and family data from the Human Connectome Project, we provide evidence that atypical language dominance is associated with global shifts in cortical organization. Individuals with atypical language organization exhibit corresponding hemispheric differences in the macroscale functional gradients that situate discrete large-scale networks along a continuous spectrum, extending from unimodal through association territories. Analyses reveal that both language lateralization and gradient asymmetries are, in part, driven by genetic factors. These findings pave the way for a deeper understanding of the origins and relationships linking population-level variability in hemispheric specialization and global properties of cortical organization. <<<

Recent work in cognitive and systems neuroscience has suggested that the hippocampus might support planning, imagination, and navigation by forming cognitive maps that capture the abstract structure of physical spaces, tasks, and situations. Navigation involves disambiguating similar contexts, and the planning and execution of a sequence of decisions to reach a goal. Here, we examine hippocampal activity patterns in humans during a goal-directed navigation task to investigate how contextual and goal information are incorporated in the construction and execution of navigational plans. During planning, hippocampal pattern similarity is enhanced across routes that share a context and a goal. During navigation, we observe prospective activation in the hippocampus that reflects the retrieval of pattern information related to a key-decision point. These results suggest that, rather than simply representing overlapping associations or state transitions, hippocampal activity patterns are shaped by context and goals. <<<

The regularities of the world render an intricate interplay between past and present. Even across independent trials, current-trial perception can be automatically shifted by preceding trials, namely the "serial bias." Meanwhile, the neural implementation of the spontaneous shift of present by past that operates on multiple features remains unknown. In two auditory categorization experiments with human electrophysiological recordings, we demonstrate that serial bias arises from the co-occurrence of past-trial neural reactivation and the neural encoding of current-trial features. The meeting of past and present shifts the neural representation of current-trial features and modulates serial bias behavior. Critically, past-trial features (i.e., pitch, category choice, motor response) keep their respective identities in memory and are only reactivated by the corresponding features in the current trial, giving rise to dissociated feature-specific serial biases. The feature-specific automatic reactivation might constitute a fundamental mechanism for adaptive past-to-present generalizations over multiple features. <<<