Goal-directed Spatial Navigation Research Articles

Disarrangement and reorganization of the hippocampal functional connectivity during the spatial path adjustment of pigeons

BackgroundThe hippocampus plays an important role to support path planning and adjustment in goal-directed spatial navigation. While we still only have limited knowledge about how do the hippocampal neural activities, especially the functional connectivity patterns, change during the spatial path adjustment. In this study, we measured the behavioural indicators and local field potentials of the pigeon (Columba livia, male and female) during a goal-directed navigational task with the detour paradigm, exploring the changing patterns of the hippocampal functional network connectivity of the bird during the spatial path learning and adjustment.ResultsOur study demonstrates that the pigeons progressively learned to solve the path adjustment task after the preferred path is blocked suddenly. Behavioural results show that both the total duration and the path lengths pigeons completed the task during the phase of adjustment are significantly longer than those during the acquisition and recovery phases. Furthermore, neural results show that hippocampal functional connectivity selectively changed during path adjustment. Specifically, we identified depressed connectivity in lower bands (delta and theta) and elevated connectivity in higher bands (slow-gamma and fast-gamma).ConclusionsThese results feature both the behavioural response and neural representation of the avian spatial cognitive learning process, suggesting that the functional disarrangement and reorganization of the connectivity in the avian hippocampus during different phases may contribute to our further understanding of the potential mechanism of path learning and adjustment.

Task-dependent mixed selectivity in the subiculum.

SummaryCA1 and subiculum (SUB) connect the hippocampus to numerous output regions. Cells in both areas have place-specific firing fields, although they are more dispersed in SUB. Weak responses to head direction and running speed have been reported in both regions. However, how such information is encoded in CA1 and SUB and the resulting impact on downstream targets are poorly understood. Here, we estimate the tuning of simultaneously recorded CA1 and SUB cells to position, head direction, and speed. Individual neurons respond conjunctively to these covariates in both regions, but the degree of mixed representation is stronger in SUB, and more so during goal-directed spatial navigation than free foraging. Each navigational variable could be decoded with higher precision, from a similar number of neurons, in SUB than CA1. The findings point to a possible contribution of mixed-selective coding in SUB to efficient transmission of hippocampal representations to widespread brain regions.

Conjunctive reward-place coding properties of dorsal distal CA1 hippocampus cells.

Autonomous motivated spatial navigation in animals or robots requires the association between spatial location and value. Hippocampal place cells are involved in goal-directed spatial navigation and the consolidation of spatial memories. Recently, Gauthier and Tank (Neuron 99(1):179-193, 2018. https://doi.org/10.1016/j.neuron.2018.06.008) have identified a subpopulation of hippocampal cells selectively activated in relation to rewarded goals. However, the relationship between these cells' spiking activity and goal representation remains elusive. We analyzed data from experiments in which rats underwent five consecutive tasks in which reward locations and spatial context were manipulated. We found CA1 populations with properties continuously ranging from place cells to reward cells. Specifically, we found typical place cells insensitive to reward locations, reward cells that only fired at correct rewarded feeders in each task regardless of context, and "hybrid cells" that responded to spatial locations and change of reward locations. Reward cells responded mostly to the reward delivery rather than to its expectation. In addition, we found a small group of neurons that transitioned between place and reward cells properties within the 5-task session. We conclude that some pyramidal cells (if not all) integrate both spatial and reward inputs to various degrees. These results provide insights into the integrative coding properties of CA1 pyramidal cells, focusing on their abilities to carry both spatial and reward information in a mixed and plastic manner. This conjunctive coding property prompts a re-thinking of current computational models of spatial navigation in which hippocampal spatial and subcortical value representations are independent.

Travel Planning Ability in Right Brain-Damaged Patients: Two Case Reports.

Planning ability is fundamental for goal-directed spatial navigation. Preliminary findings from patients and healthy individuals suggest that travel planning (TP)—namely, navigational planning—can be considered a distinct process from visuospatial planning (VP) ability. To shed light on this distinction, two right brain-damaged patients without hemineglect were compared with a control group on two tasks aimed at testing VP (i.e., Tower of London-16, ToL-16) and TP (i.e., Minefield Task, MFT). The former requires planning the moves to reach the right configuration of three colored beads on three pegs, whereas the latter was opportunely developed to assess TP in the navigational environment when obstacles are present. Specifically, the MFT requires participants to plan a route on a large carpet avoiding some hidden obstacles previously observed. Patient 1 showed lesions encompassing the temporoparietal region and the insula; she performed poorer than the control group on the ToL-16 but showed no deficit on the MFT. Conversely, Patient 2 showed lesions mainly located in the occipitoparietal network of spatial navigation; she performed worse than the control group on the MFT but not on the ToL-16. In both cases performances satisfied the criteria for a classical dissociation, meeting criteria for a double dissociation. These results support the idea that TP is a distinct ability and that it is dissociated from VP skills.

Structured inhibitory activity dynamics in new virtual environments.

Inhibition plays a powerful role in regulating network excitation and plasticity; however, the activity of defined interneuron types during spatial exploration remain poorly understood. Using two-photon calcium imaging, we recorded hippocampal CA1 somatostatin- and parvalbumin-expressing interneurons as mice performed a goal-directed spatial navigation task in new visual virtual reality (VR) contexts. Activity in both interneuron classes was strongly suppressed but recovered as animals learned to adapt the previously learned task to the new spatial context. Surprisingly, although there was a range of activity suppression across the population, individual somatostatin-expressing interneurons showed consistent levels of activity modulation across exposure to multiple novel environments, suggesting context-independent, stable network roles during spatial exploration. This work reveals population-level temporally dynamic interneuron activity in new environments, within which each interneuron shows stable and consistent activity modulation.

NavigationCircuits – Neural circuits for route planning in goal-directed spatial navigation – ERC

NavigationCircuits – Neural circuits for route planning in goal-directed spatial navigation – ERC

Assistive Device Art: aiding audio spatial location through the Echolocation Headphones

Assistive Device Art derives from the integration of Assistive Technology and Art, involving the mediation of sensorimotor functions and perception from both, psychophysical methods and conceptual mechanics of sensory embodiment. This paper describes the concept of ADA and its origins by observing the phenomena that surround the aesthetics of prosthesis-related art. It also analyzes one case study, the Echolocation Headphones, relating its provenience and performance to this new conceptual and psychophysical approach of tool design. This ADA tool is designed to aid human echolocation. They facilitate the experience of sonic vision, as a way of reflecting and learning about the construct of our spatial perception. Echolocation Headphones are a pair of opaque goggles which disable the participant’s vision. This device emits a focused sound beam which activates the space with directional acoustic reflection, giving the user the ability to navigate and perceive space through audition. The directional properties of parametric sound provide the participant a focal echo, similar to the focal point of vision. This study analyzes the effectiveness of this wearable sensory extension for aiding auditory spatial location in three experiments; optimal sound type and distance for object location, perceptual resolution by just noticeable difference, and goal-directed spatial navigation for open pathway detection, all conducted at the Virtual Reality Lab of the University of Tsukuba, Japan. The Echolocation Headphones have been designed for a diverse participant base. They have both the potential to aid auditory spatial perception for the visually impaired and to train sighted individuals in gaining human echolocation abilities. Furthermore, this Assistive Device artwork instigates participants to contemplate on the plasticity of their sensorimotor architecture.

Network mechanisms of hippocampal laterality, place coding, and goal-directed navigation.

The hippocampus and associated structures are responsible for episodic memory in humans. In rodents, the most prominent behavioral correlate of hippocampal neural activity is place coding, which is thought to underlie spatial navigation. While episodic memory is considered to be unique to humans in a restricted context, it has been proposed that the same neural circuitry and algorithms that enable spatial coding and navigation also support episodic memory. Here we review the recent progress in neural circuit mechanisms of hippocampal activity by introducing several topics: (1) cooperation and specialization of the bilateral hippocampi, (2) the role of synaptic plasticity in gamma phase-locking of spikes and place cell formation, (3) impaired goal-related activity and oscillations in a mouse model of mental disorders, and (4) a prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation.

A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation.

Spatial navigation requires information about the relationship between current and future positions. The activity of hippocampal neurons appears to reflect such a relationship, representing not only instantaneous position but also the path towards a goal location. However, how the hippocampus obtains information about goal direction is poorly understood. Here we report a prefrontal-thalamic neural circuit that is required for hippocampal representation of routes or trajectories through the environment. Trajectory-dependent firing was observed in medial prefrontal cortex, the nucleus reuniens of the thalamus, and the CA1 region of the hippocampus in rats. Lesioning or optogenetic silencing of the nucleus reuniens substantially reduced trajectory-dependent CA1 firing. Trajectory-dependent activity was almost absent in CA3, which does not receive nucleus reuniens input. The data suggest that projections from medial prefrontal cortex, via the nucleus reuniens, are crucial for representation of the future path during goal-directed behaviour and point to the thalamus as a key node in networks for long-range communication between cortical regions involved in navigation.

Lesions of the hippocampus or dorsolateral striatum disrupt distinct aspects of spatial navigation strategies based on proximal and distal information in a cued variant of the Morris water task

The hippocampus and dorsolateral striatum are critically involved in spatial navigation based on extra-maze and intra-maze cues, respectively. Previous reports from our laboratory suggest that behavior in the Morris water task may be guided by both cue types, and rats appear to switch from extra-pool to intra-pool cues to guide navigation in a sequential manner within a given trial. In two experiments, rats with hippocampal or dorsolateral striatal lesions were trained and tested in water task paradigms that involved translation and removal of a cued platform within the pool and translations of the pool itself with respect to the extra-pool cue reference frame. In the first experiment, moment-to-moment analyses of swim behavior indicate that hippocampal lesions disrupt initial trajectories based on extra-pool cues at the beginning of the trial, while dorsolateral striatal lesions disrupt subsequent swim trajectories based on the location of the cued platform at the end of the trial. In the second experiment, lesions of the hippocampus, but not the dorsolateral striatum, impaired directional responding in situations where the pool was shifted within the extra-pool cue array. These results are important for understanding the cooperative interactions between the hippocampus and dorsolateral striatum in spatial learning and memory and establish that these brain areas are continuously involved in goal-directed spatial navigation. These results also highlight the importance of the hippocampus in directional responding in addition to place navigation.

Principles of goal-directed spatial robot navigation in biomimetic models.

Mobile robots and animals alike must effectively navigate their environments in order to achieve their goals. For animals goal-directed navigation facilitates finding food, seeking shelter or migration; similarly robots perform goal-directed navigation to find a charging station, get out of the rain or guide a person to a destination. This similarity in tasks extends to the environment as well; increasingly, mobile robots are operating in the same underwater, ground and aerial environments that animals do. Yet despite these similarities, goal-directed navigation research in robotics and biology has proceeded largely in parallel, linked only by a small amount of interdisciplinary research spanning both areas. Most state-of-the-art robotic navigation systems employ a range of sensors, world representations and navigation algorithms that seem far removed from what we know of how animals navigate; their navigation systems are shaped by key principles of navigation in 'real-world' environments including dealing with uncertainty in sensing, landmark observation and world modelling. By contrast, biomimetic animal navigation models produce plausible animal navigation behaviour in a range of laboratory experimental navigation paradigms, typically without addressing many of these robotic navigation principles. In this paper, we attempt to link robotics and biology by reviewing the current state of the art in conventional and biomimetic goal-directed navigation models, focusing on the key principles of goal-oriented robotic navigation and the extent to which these principles have been adapted by biomimetic navigation models and why.

The Mixed Instrumental Controller: Using Value of Information to Combine Habitual Choice and Mental Simulation

Instrumental behavior depends on both goal-directed and habitual mechanisms of choice. Normative views cast these mechanisms in terms of model-free and model-based methods of reinforcement learning, respectively. An influential proposal hypothesizes that model-free and model-based mechanisms coexist and compete in the brain according to their relative uncertainty. In this paper we propose a novel view in which a single Mixed Instrumental Controller produces both goal-directed and habitual behavior by flexibly balancing and combining model-based and model-free computations. The Mixed Instrumental Controller performs a cost-benefits analysis to decide whether to chose an action immediately based on the available “cached” value of actions (linked to model-free mechanisms) or to improve value estimation by mentally simulating the expected outcome values (linked to model-based mechanisms). Since mental simulation entails cognitive effort and increases the reward delay, it is activated only when the associated “Value of Information” exceeds its costs. The model proposes a method to compute the Value of Information, based on the uncertainty of action values and on the distance of alternative cached action values. Overall, the model by default chooses on the basis of lighter model-free estimates, and integrates them with costly model-based predictions only when useful. Mental simulation uses a sampling method to produce reward expectancies, which are used to update the cached value of one or more actions; in turn, this updated value is used for the choice. The key predictions of the model are tested in different settings of a double T-maze scenario. Results are discussed in relation with neurobiological evidence on the hippocampus – ventral striatum circuit in rodents, which has been linked to goal-directed spatial navigation.

Modeling goal-directed spatial navigation in the rat based on physiological data from the hippocampal formation

We investigated the importance of hippocampal theta oscillations and the significance of phase differences of theta modulation in the cortical regions that are involved in goal-directed spatial navigation. Our models used representations of entorhinal cortex layer III (ECIII), hippocampus and prefrontal cortex (PFC) to guide movements of a virtual rat in a virtual environment. The model encoded representations of the environment through long-term potentiation of excitatory recurrent connections between sequentially spiking place cells in ECIII and CA3. This encoding required buffering of place cell activity, which was achieved by a short-term memory (STM) in EC that was regulated by theta modulation and allowed synchronized reactivation with encoding phases in ECIII and CA3. Inhibition at a specific theta phase deactivated the oldest item in the buffer when new input was presented to a full STM buffer. A 180° phase difference separated retrieval and encoding in ECIII and CA3, which enabled us to simulate data on theta phase precession of place cells. Retrieval of known paths was elicited in ECIII by input at the retrieval phase from PFC working memory for goal location, requiring strict theta phase relationships with PFC. Known locations adjacent to the virtual rat were retrieved in CA3. Together, input from ECIII and CA3 activated predictive spiking in cells in CA1 for the next desired place on a shortest path to a goal. Consistent with data, place cell activity in CA1 and CA3 showed smaller place fields than in ECIII.

Impaired Recognition of the Goal Location during Spatial Navigation in Rats with Hippocampal Lesions

Converging evidence suggests that the hippocampus is essential for goal-directed spatial navigation. Successful navigation requires not only the ability to compute an appropriate path toward the target but is also guided by recognition of places along the trajectory between start and goal. To determine whether the hippocampus contributes to place recognition, we trained rats with hippocampal lesions in an annular water maze with a remotely controlled escape platform at a constant location in the corridor. The platform remained submerged and unavailable until the rat had swum at least one full lap. Probe trials with the platform unavailable for 60 sec were inserted at regular intervals. In these trials, the rat would swim over the platform several times, regardless of its navigational abilities. After a few training sessions, all sham-operated control animals reduced their swim velocity when they approached the platform, indicating that they recognized the target location. Rats with hippocampal lesions, in contrast, swam at the same velocity as elsewhere in the corridor. Preoperative training or prolonged postoperative training did not alleviate the deficit. Rats with hippocampal lesions were able to learn a cued version of the task, which implies that the failure to slow down was not attributable to motor inflexibility. Thus, hippocampal lesions caused a severe but selective deficit in the identification of a location, suggesting that the hippocampus may be essential for image recognition during spatial navigation.