Medial temporal lobe roles in human path integration.

Path integration is a process in which observers derive their location by integrating self-motion signals along their locomotion trajectory. Although the medial temporal lobe (MTL) is thought to take part in path integration, the scope of its role for path integration remains unclear. To address this issue, we administered a variety of tasks involving path integration and other related processes to a group of neurosurgical patients whose MTL was unilaterally resected as therapy for epilepsy. These patients were unimpaired relative to neurologically intact controls in many tasks that required integration of various kinds of sensory self-motion information. However, the same patients (especially those who had lesions in the right hemisphere) walked farther than the controls when attempting to walk without vision to a previewed target. Importantly, this task was unique in our test battery in that it allowed participants to form a mental representation of the target location and anticipate their upcoming walking trajectory before they began moving. Thus, these results put forth a new idea that the role of MTL structures for human path integration may stem from their participation in predicting the consequences of one's locomotor actions. The strengths of this new theoretical viewpoint are discussed.

The role of spatial memory and frames of reference in the precision of angular path integration.

Angular path integration refers to the ability to maintain an estimate of self-location after a rotational displacement by integrating internally-generated (idiothetic) self-motion signals over time. Previous work has found that non-sensory inputs, namely spatial memory, can play a powerful role in angular path integration (Arthur et al., 2007, 2009). Here we investigated the conditions under which spatial memory facilitates angular path integration. We hypothesized that the benefit of spatial memory is particularly likely in spatial updating tasks in which one's self-location estimate is referenced to external space. To test this idea, we administered passive, non-visual body rotations (ranging 40°-140°) about the yaw axis and asked participants to use verbal reports or open-loop manual pointing to indicate the magnitude of the rotation. Prior to some trials, previews of the surrounding environment were given. We found that when participants adopted an egocentric frame of reference, the previously-observed benefit of previews on within-subject response precision was not manifested, regardless of whether remembered spatial frameworks were derived from vision or spatial language. We conclude that the powerful effect of spatial memory is dependent on one's frame of reference during self-motion updating.

Linear path integration deficits in patients with abnormal vestibular afference.

Effective navigation requires the ability to keep track of one's location and maintain orientation during linear and angular displacements. Path integration is the process of updating the representation of body position by integrating internally-generated self-motion signals over time (e.g., walking in the dark). One major source of input to path integration is vestibular afference. We tested patients with reduced vestibular function (unilateral vestibular hypofunction, UVH), patients with aberrant vestibular function (benign paroxysmal positional vertigo, BPPV), and healthy participants (controls) on two linear path integration tasks: experimenter-guided walking and target-directed walking. The experimenter-guided walking task revealed a systematic underestimation of self-motion signals in UVH patients compared to the other groups. However, we did not find any difference in the distance walked between the UVH group and the control group for the target-directed walking task. Results from neuropsychological testing and clinical balance measures suggest that the errors in experimenter-guided walking were not attributable to cognitive and/or balance impairments. We conclude that impairment in linear path integration in UVH patients stem from deficits in self-motion perception. Importantly, our results also suggest that patients with a UVH deficit do not lose their ability to walk accurately without vision to a memorized target location.

Non-sensory inputs to angular path integration.

Non-sensory (cognitive) inputs can play a powerful role in monitoring one's self-motion. Previously, we showed that access to spatial memory dramatically increases response precision in an angular self-motion updating task [1]. Here, we examined whether spatial memory also enhances a particular type of self-motion updating - angular path integration. "Angular path integration" refers to the ability to maintain an estimate of self-location after a rotational displacement by integrating internally-generated (idiothetic) self-motion signals over time. It was hypothesized that remembered spatial frameworks derived from vision and spatial language should facilitate angular path integration by decreasing the uncertainty of self-location estimates. To test this we implemented a whole-body rotation paradigm with passive, non-visual body rotations (ranging 40 degrees -140 degrees ) administered about the yaw axis. Prior to the rotations, visual previews (Experiment 1) and verbal descriptions (Experiment 2) of the surrounding environment were given to participants. Perceived angular displacement was assessed by open-loop pointing to the origin (0 degrees ). We found that within-subject response precision significantly increased when participants were provided a spatial context prior to whole-body rotations. The present study goes beyond our previous findings by first establishing that memory of the environment enhances the processing of idiothetic self-motion signals. Moreover, we show that knowledge of one's immediate environment, whether gained from direct visual perception or from indirect experience (i.e., spatial language), facilitates the integration of incoming self-motion signals.

Progressive locomotor recalibration during blind walking.

Blind walking has become a common measure of perceived target location. This article addresses the possibility that blind walking might vary systematically within an experimental session as participants accrue exposure to nonvisual locomotion. Such variations could complicate the interpretation of blind walking as a measure of perceived location. We measured walked distance, velocity, and pace length in indoor and outdoor environments (1.5-16.0 m target distances). Walked distance increased over 37 trials by approximately 9.33% of the target distance; velocity (and to a lesser extent, pace length) also increased, primarily in the first few trials. In addition, participants exhibited more unintentional forward drift in a blindfolded marching-in-place task after exposure to nonvisual walking. The results suggest that participants not only gain confidence as blind-walking exposure increases, but also adapt to nonvisual walking in a way that biases responses toward progressively longer walked distances.

Exploring the process of progressive disorientation.

While an increasing number of behavioral studies examining spatial cognition use experimental paradigms involving disorientation, the process by which one becomes disoriented is not well explored. The current study examined this process using a paradigm in which participants were blindfolded and underwent a succession of 70 degrees or 200 degrees passive, whole body rotations around a fixed vertical axis. After each rotation, participants used a pointer to indicate either their heading at the start of the most recent turn or their heading at the start of the current series of turns. Analyses showed that in both cases, mean pointing errors increased gradually over successive turns. In addition to the gradual loss of orientation indicated by this increase, analysis of the pointing errors also showed evidence of occasional, abrupt loss orientation. Results indicate multiple routes from an oriented to a disoriented state, and shed light on the process of becoming disoriented.

Misperception of exocentric directions in auditory space.

Previous studies have demonstrated large errors (over 30 degrees ) in visually perceived exocentric directions (the direction between two objects that are both displaced from the observer's location; e.g., Philbeck et al. [Philbeck, J. W., Sargent, J., Arthur, J. C., & Dopkins, S. (2008). Large manual pointing errors, but accurate verbal reports, for indications of target azimuth. Perception, 37, 511-534]). Here, we investigated whether a similar pattern occurs in auditory space. Blindfolded participants either attempted to aim a pointer at auditory targets (an exocentric task) or gave a verbal estimate of the egocentric target azimuth. Targets were located at 20-160 degrees azimuth in the right hemispace. For comparison, we also collected pointing and verbal judgments for visual targets. We found that exocentric pointing responses exhibited sizeable undershooting errors, for both auditory and visual targets, that tended to become more strongly negative as azimuth increased (up to -19 degrees for visual targets at 160 degrees ). Verbal estimates of the auditory and visual target azimuths, however, showed a dramatically different pattern, with relatively small overestimations of azimuths in the rear hemispace. At least some of the differences between verbal and pointing responses appear to be due to the frames of reference underlying the responses; when participants used the pointer to reproduce the egocentric target azimuth rather than the exocentric target direction relative to the pointer, the pattern of pointing errors more closely resembled that seen in verbal reports. These results show that there are similar distortions in perceiving exocentric directions in visual and auditory space.

Large manual pointing errors, but accurate verbal reports, for indications of target azimuth.

Many tasks have been used to probe human directional knowledge, but relatively little is known about the comparative merits of different means of indicating target azimuth. Few studies have compared action-based versus non-action-based judgments for targets encircling the observer. This comparison promises to illuminate not only the perception of azimuths in the front and rear hemispaces, but also the frames of reference underlying various azimuth judgments, and ultimately their neural underpinnings. We compared a response in which participants aimed a pointer at a nearby target, with verbal azimuth estimates. Target locations were distributed between 20 degrees and 340 degrees. Non-visual pointing responses exhibited large constant errors (up to -32 degrees) that tended to increase with target eccentricity. Pointing with eyes open also showed large errors (up to -21 degrees). In striking contrast, verbal reports were highly accurate, with constant errors rarely exceeding +/-5 degrees. Under our testing conditions, these results are not likely to stem from differences in perception-based versus action-based responses, but instead reflect the frames of reference underlying the pointing and verbal responses. When participants used the pointer to match the egocentric target azimuth rather than the exocentric target azimuth relative to the pointer, errors were reduced.

Spatial memory enhances the precision of angular self-motion updating.

Humans are typically able to keep track of brief changes in their head and body orientation, even when visual and auditory cues are temporarily unavailable. Determining the magnitude of one's displacement from a known location is one form of self-motion updating. Most research on self-motion updating during body rotations has focused on the role of a restricted set of sensory signals (primarily vestibular) available during self-motion. However, humans can and do internally represent spatial aspects of the environment, and little is known about how remembered spatial frameworks may impact angular self-motion updating. Here, we describe an experiment addressing this issue. Participants estimated the magnitude of passive, non-visual body rotations (40 degrees -130 degrees ), using non-visual manual pointing. Prior to each rotation, participants were either allowed full vision of the testing environment, or remained blindfolded. Within-subject response precision was dramatically enhanced when the body rotations were preceded by a visual preview of the surrounding environment; constant (signed) and absolute (unsigned) error were much less affected. These results are informative for future perceptual, cognitive, and neuropsychological studies, and demonstrate the powerful role of stored spatial representations for improving the precision of angular self-motion updating.