Functional MRI investigations of path integration and goal-directed navigation in humans

Path integration is a navigational process that humans and animals use to track changes in their position and orientation. Animal and computational studies suggest that a spatially-tuned navigation system supports path integration, yet this system is not well understood in humans. Here, the prediction was tested that path integration mechanisms and goal-directed navigation in humans would recruit the same key brain regions within the parietal cortex and medial temporal lobes as predicted by animal and computational models. The three experiments described in this dissertation used behavioral and functional magnetic resonance imaging methods in 131 adults (18-35 years) to examine behavioral and brain correlates of navigation. In a landmark-free environment, path integration mechanisms are utilized to update position and orientation to a goal. Experiment 1 examined neural correlates of these mechanisms in the human brain. The results demonstrated that successful first and third person perspective navigation recruited the anterior hippocampus. The posterior hippocampus was found to track distance and temporal proximity to a goal location. The retrosplenial and posterior parietal cortices were additionally recruited for successful goal-directed navigation. In a landmark-rich environment, humans utilize route-based strategies to triangulate between their position, landmarks, and navigational goal. Experiment 2 contrasted path integration and landmark-based strategies by adding a solitary landmark to a sparse environment. The results demonstrated that successful navigation with and without an orienting landmark recruited the anterior hippocampus. Activity in the bilateral posterior hippocampus was modulated by larger triangulation between current position, landmark, and goal location during first person perspective navigation. The caudate nucleus was additionally recruited for landmark-based navigation. Experiment 3 used functional connectivity methods coupled with two fMRI tasks to determine whether areas responsive to optic flow, specifically V3A, V6, and the human motion complex (hMT+), are functionally connected to brain regions recruited during first person perspective navigation. The results demonstrated a functional relationship between optic flow areas and navigationally responsive regions, including the hippocampus, retrosplenial, posterior parietal, and medial prefrontal cortices. These studies demonstrate that goal-directed navigation is reliant upon a navigational system supported by hippocampal position computations and orientation calculations from the retrosplenial and posterior parietal cortices

Functional organization of the caudal part of the human superior parietal lobule

: Like in macaque, the caudal portion of the human superior parietal lobule (SPL) plays a key role in a series of perceptive, visuomotor and somatosensory processes. Here, we review the functional properties of three separate portions of the caudal SPL, i.e., the posterior parieto-occipital sulcus (POs), the anterior POs, and the anterior part of the caudal SPL. We propose that the posterior POs is mainly dedicated to the analysis of visual motion cues useful for object motion detection during self-motion and for spatial navigation, while the more anterior parts are implicated in visuomotor control of limb actions. The anterior POs is mainly involved in using the spotlight of attention to guide reach-to-grasp hand movements, especially in dynamic environments. The anterior part of the caudal SPL plays a central role in visually guided locomotion, being implicated in controlling leg-related movements as well as the four limbs interaction with the environment, and in encoding egomotion-compatible optic flow. Together, these functions reveal how the caudal SPL is strongly implicated in skilled visually-guided behaviors

A common neural substrate for processing scenes and egomotion-compatible visual motion

Neuroimaging studies have revealed two separate classes of category-selective regions specialized in optic flow (egomotion-compatible) processing and in scene/place perception. Despite the importance of both optic flow and scene/place recognition to estimate changes in position and orientation within the environment during self-motion, the possible functional link between egomotion- and scene-selective regions has not yet been established. Here we reanalyzed functional magnetic resonance images from a large sample of participants performing two well-known “localizer” fMRI experiments, consisting in passive viewing of navigationally relevant stimuli such as buildings and places (scene/place stimulus) and coherently moving fields of dots simulating the visual stimulation during self-motion (flow fields). After interrogating the egomotion-selective areas with respect to the scene/place stimulus and the scene-selective areas with respect to flow fields, we found that the egomotion-selective areas V6+ and pIPS/V3A responded bilaterally more to scenes/places compared to faces, and all the scene-selective areas (parahippocampal place area or PPA, retrosplenial complex or RSC, and occipital place area or OPA) responded more to egomotion-compatible optic flow compared to random motion. The conjunction analysis between scene/place and flow field stimuli revealed that the most important focus of common activation was found in the dorsolateral parieto-occipital cortex, spanning the scene-selective OPA and the egomotion-selective pIPS/V3A. Individual inspection of the relative locations of these two regions revealed a partial overlap and a similar response profile to an independent low-level visual motion stimulus, suggesting that OPA and pIPS/V3A may be part of a unique motion-selective complex specialized in encoding both egomotion- and scene-relevant information, likely for the control of navigation in a structured environment

A common neural substrate for processing scenes and egomotion-compatible visual motion

Neuroimaging studies have revealed two separate classes of category-selective regions specialized in optic flow (egomotion-compatible) processing and in scene/place perception. Despite the importance of both optic flow and scene/place recognition to estimate changes in position and orientation within the environment during self-motion, the possible functional link between egomotion- and scene-selective regions has not yet been established. Here we reanalyzed functional magnetic resonance images from a large sample of participants performing two well-known \u201clocalizer\u201d fMRI experiments, consisting in passive viewing of navigationally relevant stimuli such as buildings and places (scene/place stimulus) and coherently moving fields of dots simulating the visual stimulation during self-motion (flow fields). After interrogating the egomotion-selective areas with respect to the scene/place stimulus and the scene-selective areas with respect to flow fields, we found that the egomotion-selective areas V6+ and pIPS/V3A responded bilaterally more to scenes/places compared to faces, and all the scene-selective areas (parahippocampal place area or PPA, retrosplenial complex or RSC, and occipital place area or OPA) responded more to egomotion-compatible optic flow compared to random motion. The conjunction analysis between scene/place and flow field stimuli revealed that the most important focus of common activation was found in the dorsolateral parieto-occipital cortex, spanning the scene-selective OPA and the egomotion-selective pIPS/V3A. Individual inspection of the relative locations of these two regions revealed a partial overlap and a similar response profile to an independent low-level visual motion stimulus, suggesting that OPA and pIPS/V3A may be part of a unique motion-selective complex specialized in encoding both egomotion- and scene-relevant information, likely for the control of navigation in a structured environment

Maps and memories of space in the human brain

Mammalian navigation is mostly studied in rodents and humans. Due to ethical and methodological constraints, rodent research so far primarily targeted the neurophysiological mechanisms of navigation, while navigation studies in humans predominantly focused on navigational behavior and the cognitive processes involved in it. Although basic mechanisms of navigation seem well preserved across rodents and humans in general, human and rodent navigation also differ substantially in several aspects and it is not obvious how particular findings translate across both species. As a consequence, for many aspects of navigation, we do not know how processes on the cognitive level can be attributed to those on the cellular level, and, eventually, how particular navigation behavior can be causally related to neural activity. This knowledge gap is addressed in this thesis with two studies that extend our understanding of how findings from rodents and humans translate across both species. To this end, a framework was developed that combines human navigation in landmark-sparse virtual environments that resemble the open-field setups typically used to study spatially tuned neurons in rodents. Applying this framework, the first study presented in this thesis separates passive and active components during navigation, and investigates how varying navigational and spatial memory demands impact participants' brain activity. The results suggest that, first, certain brain regions primarily known for perception of static scenes are recruited during passive navigation, and also contribute information processing specifically relevant for active navigation; and that, second, the anterior medial hippocampus provides a coherent spatial representation of the current environment that is dependent on spatial memory. Using a similar setup, the second study investigates participants' spatial representation in more detail. The results show that, first, a model inspired by electrophysiological findings in rodents that explains location memory as a function of proximity to the environment's boundaries generally matches participants' behavior in a similar open-field environment; that, second, the model's explanatory power may be further improved when, in addition to the precision, also the accuracy of participants' location memory is considered; and that, finally, in a quadratic open-field environment, the diagonals also impact participant's spatial orientation and location memory. The findings reported in this thesis demonstrate that the framework applied in both studies allows for a detailed investigation of human navigation behavior, and the cognitive processes associated with it. It furthermore increases comparability of findings between human and rodent navigation, and may eventually help to better understand how neurophysiological processes are transformed into navigation behavior

The human posterior cingulate, retrosplenial, and medial parietal cortex effective connectome, and implications for memory and navigation

The human posterior cingulate, retrosplenial, and medial parietal cortex are involved in memory and navigation. The functional anatomy underlying these cognitive functions was investigated by measuring the effective connectivity of these Posterior Cingulate Division (PCD) regions in the Human Connectome Project-MMP1 atlas in 171 HCP participants, and complemented with functional connectivity and diffusion tractography. First, the postero-ventral parts of the PCD (31pd, 31pv, 7m, d23ab, and v23ab) have effective connectivity with the temporal pole, inferior temporal visual cortex, cortex in the superior temporal sulcus implicated in auditory and semantic processing, with the reward-related vmPFC and pregenual anterior cingulate cortex, with the inferior parietal cortex, and with the hippocampal system. This connectivity implicates it in hippocampal episodic memory, providing routes for “what,” reward and semantic schema-related information to access the hippocampus. Second, the antero-dorsal parts of the PCD (especially 31a and 23d, PCV, and also RSC) have connectivity with early visual cortical areas including those that represent spatial scenes, with the superior parietal cortex, with the pregenual anterior cingulate cortex, and with the hippocampal system. This connectivity implicates it in the “where” component for hippocampal episodic memory and for spatial navigation. The dorsal–transitional–visual (DVT) and ProStriate regions where the retrosplenial scene area is located have connectivity from early visual cortical areas to the parahippocampal scene area, providing a ventromedial route for spatial scene information to reach the hippocampus. These connectivities provide important routes for “what,” reward, and “where” scene-related information for human hippocampal episodic memory and navigation. The midcingulate cortex provides a route from the anterior dorsal parts of the PCD and the supracallosal part of the anterior cingulate cortex to premotor regions

Anchoring The Cognitive Map To The Visual World

To interact rapidly and effectively with the environment, the mammalian brain needs a representation of the spatial layout of the external world (or a “cognitive map”). A person might need to know where she is standing to find her way home, for instance, or might need to know where she is looking to reach for her out-of-sight keys. For many behaviors, however, simply possessing a map is not enough; in order for a map to be useful in a dynamic world, it must be anchored to stable environmental cues. The goal of the present research is to address this spatial anchoring problem in two different domains: navigation and vision. In the first part of the thesis, which comprises Chapters 1-3, we examine how navigators use perceptual information to re-anchor their cognitive map after becoming lost, a process known as spatial reorientation. Using a novel behavioral paradigm with rodents, in Chapter 2 we show that the cognitive map is reoriented by dissociable inputs for identifying where one is and recovering which way one is facing. The findings presented in Chapter 2 also highlight the importance of environmental boundaries, such as the walls of a room, for anchoring the cognitive map. We thus predicted that there might exist a brain region that is selectively involved in boundary perception during navigation. Accordingly, in Chapter 3, we combine transcranial magnetic stimulation and virtual-reality navigation to reveal the existence of such a boundary perception region in humans. In the second part of this thesis, Chapter 4, we explore whether the same mechanisms that support the cognitive map of navigational space also mediate a map of visual space (i.e., where one is looking). Using functional magnetic resonance imaging and eye tracking, we show that human entorhinal cortex supports a map-like representation of visual space that obeys the same principles of boundary-anchoring previously observed in rodent maps of navigational space. Together, this research elucidates how mental maps are anchored to the world, thus allowing the mammalian brain to form durable spatial representations across body and eye movements

Neurons including hippocampal spatial view cells, and navigation in primates including humans

A new theory is proposed of mechanisms of navigation in primates including humans in which spatial view cells found in the primate hippocampus and parahippocampal gyrus are used to guide the individual from landmark to landmark. The navigation involves approach to each landmark in turn (taxis), using spatial view cells to identify the next landmark in the sequence, and does not require a topological map. Two other cell types found in primates, whole body motion cells, and head direction cells, can be utilized in the spatial view cell navigational mechanism, but are not essential. If the landmarks become obscured, then the spatial view representations can be updated by self‐motion (idiothetic) path integration using spatial coordinate transform mechanisms in the primate dorsal visual system to transform from egocentric to allocentric spatial view coordinates. A continuous attractor network or time cells or working memory is used in this approach to navigation to encode and recall the spatial view sequences involved. I also propose how navigation can be performed using a further type of neuron found in primates, allocentric‐bearing‐to‐a‐landmark neurons, in which changes of direction are made when a landmark reaches a particular allocentric bearing. This is useful if a landmark cannot be approached. The theories are made explicit in models of navigation, which are then illustrated by computer simulations. These types of navigation are contrasted with triangulation, which requires a topological map. It is proposed that the first strategy utilizing spatial view cells is used frequently in humans, and is relatively simple because primates have spatial view neurons that respond allocentrically to locations in spatial scenes. An advantage of this approach to navigation is that hippocampal spatial view neurons are also useful for episodic memory, and for imagery

Making a stronger case for comparative research to investigate the behavioral and neurological bases of three-dimensional navigation

The rich diversity of avian natural history provides exciting possibilities for comparative research aimed at understanding three-dimensional navigation. We propose some hypotheses relating differences in natural history to potential behavioral and neurological adaptations possessed by contrasting bird species. This comparative approach may offer unique insights into some of the important questions raised by Jeffery et al

The role of global motion perception and cortical visual motion area dynamics in visual path integration in cognitively intact aged adults

Spatial navigation is a cognitive skill fundamental to successful interaction with our environment. Normal aging is associated with weaknesses in this skill, with severe deficits in the context of Alzheimer's disease. Identifying mechanisms underlying how the aged brain navigates is important to understanding these age-related weaknesses and potentially strengthening or preserving spatial navigation ability in the aging population. One understudied aspect of spatial navigation is self-motion perception. Important to self-motion perception is optic flow, which is the pattern of visual motion experienced while moving through our environment. Several brain regions are optic flow-sensitive (OF-sensitive), responding more strongly to optic flow than other types of visual motion. The goal of the experiments in this dissertation was to examine the role of visual motion perception and cortical motion area dynamics in spatial navigation in cognitively intact aged adults. Visual path integration tasks were used because they highlight the use of radial and translational optic flow to keep track of one’s position and orientation, respectively. In the first experiment, a positive relationship between radial optic flow sensitivity and visual path integration accuracy that was stronger in aged adults was found. In the second experiment, brain activity was measured using functional magnetic resonance imaging (fMRI) while participants performed visual path integration (VPI) and turn counting (TC) tasks. Stronger activity in the OF-sensitive regions LMT+ and RpVIP during VPI, not TC, was associated with greater VPI accuracy in aged adults. In the third experiment, the functional connectivity between OF-sensitive regions and the rest of the brain during the VPI and TC tasks was measured using fMRI. Stronger average functional connectivity between the OF-sensitive regions LMT+, RMT+, LpVIP, RpVIP, LpV6 and right supramarginal gyrus and posterior cingulate during VPI, not TC, was associated with greater VPI task accuracy in aged adults. The results demonstrate novel relationships between visual path integration accuracy and radial motion perception, the response of OF-sensitive cortical regions during visual navigation, and the interaction strength between OF-sensitive regions and parietal cortex during visual navigation in aged adults. This work expands our knowledge of mechanisms underlying spatial navigation processes in the aged human brain