Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions

The cingulate cortex plays a central role in bridging neocortical and limbic structures involved in allothetic navigation, a form of navigation requiring the use of external cues. Animals can also navigate using idiothetic cues, which are cues generated by self-movement, but there have been no definitive tests of whether cingulate cortex also plays a role in idiothetic navigation. Rats with anterior cingulate (medial frontal) and posterior cingulate cortex (retrosplenial) suction ablations were trained to search for large food pellets on an open table, and the accuracy with which they returned home with the food was measured. In the idiothetic task they searched for food from a novel starting location under infrared light, and with surface olfactory cues displaced. The rats also received two tests of allothetic navigation. They were tested on a matching-to-place task in which they foraged for food from a number of successively presented new locations under normal room light, and they were trained to locate a hidden platform in a swimming pool (Morris place task). The group with posterior cingulate cortex lesions was severely impaired on all of the navigation tasks whereas the group with anterior cingulate cortex lesions displayed no deficit on the idiothetic task and only moderate deficits on the other tasks. The results demonstrate a role for posterior cingulate region in idiothetic navigation.     

Dead reckoning (path integration) requires the hippocampal formation: evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests.

Animals navigate using cues generated by their own movements (self-movement cues or idiothetic cues), as well as the cues they encounter in their environment (distal cues or allothetic cues). Animals use these cues to navigate in two different ways. When dead reckoning (deduced reckoning or path integration), they integrate self-movement cues over time to locate a present position or to return to a starting location. When piloting, they use allothetic cues as beacons, or they use the relational properties of allothetic cues to locate places in space. The neural structures involved in cue use and navigational strategies are still poorly understood, although considerable attention is directed toward the contributions of the hippocampal formation (hippocampus and associated pathways and structures, including the fimbria-fornix and the retrosplenial cortex). In the present study, using tests in allothetic and idiothetic paradigms, we present four lines of evidence to support the hypothesis that the hippocampal formation plays a central role in dead reckoning. (1) Control but not fimbria-fornix lesion rats can return to a novel refuge location in both light and dark (infrared) food carrying tasks. (2). Control but not fimbria-fornix lesion rats make periodic direct high velocity returns to a starting location in both light and dark exploratory tests. Control but not fimbria-fornix rats trained in the light to carry food from a fixed location to a refuge are able to maintain accurate outward and homebound trajectories when tested in the dark. (3). Control but not fimbria-fornix rats are able to correct an outward trajectory to a food source when the food source is moved when allothetic cues are present. These, tests of spontaneous exploration and foraging suggest a role for the hippocampal formation in dead reckoning.     

A battery of tests for quantitative examination of idiothetic and allothetic place navigation modes in humans

Research into the neural mechanisms of place navigation in laboratory animals has led to the definition of allothetic and idiothetic navigation modes that can be examined by quantitative analysis of the generated tracks. In an attempt to use this approach in the study of human navigation behavior, 10 young subjects were examined in an enclosed arena (2.9 m in diameter, 3 m high) equipped with a computerized tracking system. Idiothetic navigation was studied in blindfolded subjects performing the following tasks-Simple Homing, Complex Homing and Idiothesis Supported by Floor-Related Signals. Allothetic navigation was examined in sighted subjects instructed to find in an empty arena the acoustically signaled unmarked goal region and later to retrieve its position using tasks (Natural Navigation, Cue-Controlled Navigation, Snapshot Memory, Map Reading) that evaluated different aspects of allothesis. The results indicate that allothetic navigation is more accurate than idiothetic, that the poor accuracy of idiothesis is due to angular rather than to distance errors, and that navigation performance is best when both allothetic and idiothetic modes contribute to the solution of the task. The proposed test battery may contribute to better understanding of the navigation disturbances accompanying various neurological disorders and to objective evaluation of the results of drug therapy and of rehabilitation procedures.     

Rats can track odors, other rats, and themselves: implications for the study of spatial behavior

In order to demonstrate that rats solve dead reckoning (path integration) tasks in which they return to a starting location using self-movement (idiothetic) cues, it is necessary to remove external (allothetic) cues. Odor cues, especially those generated by a rat on a single passage, are difficult to control and they can potentially serve as a cue to guide a homeward trip. Because it is presently unknown whether rats can track the cues that they themselves leave, as opposed to the odor trails left by other rats, we investigated this question in the present study. A tracking task was used in which rats: (1) followed a scented string from a refuge to obtain a food pellet located on a large circular table; (2) followed odors left on the table; (3) followed odors left by the passage of another rat; or (4) followed odors left by themselves. Groups of rats were presented with strings scented with either the rat's own odor (Group Own), a conspecific's odor (Group Other), or another scent, vanilla (Group Vanilla). After training, a series of discrimination tests were given to determine the nature of the stimulus that controls scent tracking. The results indicated that Own, Other, and Vanilla groups were equally proficient in discriminating and following their respective odors. The rats were also able to follow odor trails on the table surface as well as a trail left by the single passage of another rat or their own passage. This is the first study to demonstrate that rats can discriminate between conspecific odors and their own odor left during a single passage. The results are discussed in relation to their implications for experimental methodology and olfactory contributions to spatial navigation in general and dead reckoning in particular.     

Place-related neural responses in the monkey hippocampal formation in a virtual space

Place cells in the rodent hippocampal formation (HF) are suggested to be the neural substrate for a spatial cognitive map. This specific spatial property of the place cells are regulated by both allothetic cues (i.e., intramaze local and distal cues) as well as idiothetic sensory inputs; the context signaled by the distal cues allows local and idiothetic cues to be employed for spatial tuning within the maze. To investigate the effects of distal cues on place-related activity of primate HF neurons, 228 neurons were recorded from the monkey HF during virtual navigation in a similar situation to a rodent water maze, in which distal cues were important to locate the animal's position. A subset of 72 neurons displayed place-related activity in one or more virtual spaces. Most place-related responses disappeared or changed their spatial tuning (i.e., remapping) when the arrangements of the distal cues were altered/moved in the virtual spaces. These specific features of the monkey HF might underlie neurophysiological bases of human episodic memory.     

Geometric information is required for allothetic navigation in mice

In tasks for allothetic navigation, animals should orientate by means of distal cues. We have previously shown that mice use several forms of information to navigate, among which geometry, i.e. the shape of the environment, seems to play an important role. Here we investigated whether geometric features of the environment are necessary for allothetic navigation in mice. Mice were trained to navigate in a circular water maze by means of four distal landmarks distributed either symmetrically (symmetry group) or asymmetrically (asymmetry group) around the maze. Thus, mice could locate a hidden platform by either differentiating the landmarks based on their intrinsic features (symmetry group) or in addition by geometric information, i.e. based on the relative distances between landmarks (asymmetry group). Data indicated that place learning occurred only in the asymmetry group. The results support the idea that mice navigate by using the relational properties between distal landmarks and that geometric information is required for proper allothetic navigation in this species.     

Relative contribution of allothetic and idiothetic navigation to place avoidance on stable and rotating arenas in darkness.

In the absence of useful visual or other exteroceptive cues, rats can orient in their environment using idiothetic navigation, the process in which the information generated during self-motion is integrated to yield a homing vector leading the animal back to a point of departure. If perceivable exteroceptive cues in the visited environment are available, their spatial relationship is integrated with idiothetic information and stored in a cognitive map of the environment. Our previous experiments demonstrated that place navigation in rats is severely impaired after devaluation of the intramaze substratal information by shuffling, i.e. by its random displacement relative to the already traversed track. Several interpretative difficulties of the previous study have been eliminated in the present study by the use of an advanced version of the shuffling apparatus. The results show that shuffling-induced impairment of substratal idiothesis depends on the salience of intramaze cues, that on a stable featureless arena, idiothesis can be updated by non-visual allothetic cues, and that shuffling exposing the animal to sudden accelerations and decelerations interferes with idiothetic navigation by the inherent conflict between substratal and inertial idiothesis. It is concluded that pure substratal idiothesis not updated by extramaze and intramaze cues cannot provide reliable navigation over distances longer than 5 m.     

Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation

Rats with dorsal hippocampus or associative parietal cortex (APC) lesions and sham-operated controls were trained on variants of the Morris water maze navigation task. In the 'proximal landmark condition', the rats had to localize the hidden platform solely on the basis of three salient object landmarks placed directly in the swimming pool. In the 'distal landmark condition', rats could rely only on distal landmarks (room cues) to locate the platform. In the 'beacon condition', the platform location was signaled by a salient cue directly attached to it. Rats with hippocampal lesions were impaired in the distal and to a less extent in the proximal landmark condition whereas rats with parietal lesions were impaired only in the proximal landmark condition. None of the lesioned groups was impaired in the beacon condition. These results suggest that the processing of information related to proximal, distal landmarks or associated beacon are mediated by different neural systems. The hippocampus would contribute to both proximal and distal landmark processing whereas the APC would be involved in the processing of proximal landmarks only. Navigation relying on a cued-platform would not require participation of the hippocampus nor the APC. Assuming that the processing of proximal landmarks heavily depends on the integration of visuospatial and idiothetic information, these results are consistent with the hypothesis that the APC plays a role in the combination of multiple sensory information and contributes to the formation of an allocentric spatial representation.     

Otolithic information is required for homing in the mouse

Navigation and the underlying brain signals are influenced by various allothetic and idiothetic cues, depending on environmental conditions and task demands. Visual landmarks typically control navigation in familiar environments but, in the absence of landmarks, self‐movement cues are able to guide navigation relatively accurately. These self‐movement cues include signals from the vestibular system, and may originate in the semicircular canals or otolith organs. Here, we tested the otolithic contribution to navigation on a food‐hoarding task in darkness and in light. The dark test prevented the use of visual cues and thus favored the use of self‐movement information, whereas the light test allowed the use of both visual and non‐visual cues. In darkness, tilted mice made shorter‐duration stops during the outward journey, and made more circuitous homeward journeys than control mice; heading error, trip duration, and peak error were greater for tilted mice than for controls. In light, tilted mice also showed more circuitous homeward trips, but appeared to correct for errors during the journey; heading error, trip duration, and peak error were similar between groups. These results suggest that signals from the otolith organs are necessary for accurate homing performance in mice, with the greatest contribution in non‐visual environments. © 2015 Wiley Periodicals, Inc.     

Effects of post-training lesions in the hippocampus and the parietal cortex on idiothetic information processing in the rat

Dead reckoning can be defined as the ability to navigate using idiothetic information based on self-movement cues without using allothetic information such as environmental cues. In the present study, we investigated the effects of hippocampal and parietal cortex lesions on homing behavior using dead reckoning in rats. Experimentally naive Wistar rats were trained with a homing task in which rats were required to take a food pellet from a cup in the arena and to return home with the pellet. After training, rats were divided into a control (CONT) group (n = 16), hippocampal lesioned (HIPP) group (n = 16), and parietal cortex lesioned (PARC) group (n = 16), and rats in the lesioned groups underwent surgery. After surgery, Test 1 (with four cups) and Test 2 (with one cup but the outgoing path was diverted by a barrier) were conducted. The HIPP group showed severe impairment in homing, but the performance of the PARC group did not differ from that of the CONT group. HIPP rats either approached wrong doors or ate the pellet in the arena. Circular statistics showed that homing directions of CONT and PARC rats showed concentration towards home, whereas those of HIPP rats did not. Our results exhibiting HIPP rats' failure in homing agree with many previous studies, but the results obtained from PARC rats were different from previous studies. These results indicate that the intact hippocampus is important for dead reckoning, but the role of the parietal cortex in dead reckoning is still not clear.     

The effects of overtraining in the Morris water maze on allocentric and egocentric learning strategies in rats

Animals can use both allocentric and egocentric strategies to learn a spatial task. Our results suggest that allocentric cues are more dominant than idiothetic cues in guiding navigation. Animals do not necessarily learn an egocentric strategy automatically, instead they probably hold just one solution to any particular task at a time until forced to learn an alternative strategy. Further, with overtraining animals do not always switch from allocentric to an egocentric learning strategy perhaps challenging suggestions of a stored hierarchy of strategies.     

Path integration in mammals

It is often assumed that navigation implies the use, by animals, of landmarks indicating the location of the goal. However, many animals (including humans) are able to return to the starting point of a journey, or to other goal sites, by relying on self-motion cues only. This process is known as path integration, and it allows an agent to calculate a route without making use of landmarks. We review the current literature on path integration and its interaction with external, location-based cues. Special importance is given to the correlation between observable behavior and the activity pattern of particular neural cell populations that implement the internal representation of space. In mammals, the latter may well be the first high-level cognitive representation to be understood at the neural level.     

NMDA lesions of Ammon's horn and the dentate gyrus disrupt the direct and temporally paced homing displayed by rats exploring a novel environment: evidence for a role of the hippocampus in dead reckoning

Dead reckoning, a form of navigation used to locate a present position and to return to a starting position, is used by rats to return to their home base. The present experiment examined whether dead reckoning is displayed by rats during their first exploratory excursions in a novel environment and also examined whether the behaviour requires the integrity of the cells of the hippocampus. Experimental rats, those with NMDA (N-methyl d-aspartate) lesions of Ammon's horn and the dentate gyrus, and control rats could leave a cage to explore a large circular table under light and dark conditions. Home base behaviour, use of olfactory cues, and thigmotaxic- based navigation were evaluated. Temporal, topographical and kinematic analyses were conducted on the first three exploratory excursions that extended at least halfway across the table. Groups did not differ in numbers of exits from the home base, lingering near the home base, distance travelled, or the use of surface cues as might be exemplified by thigmotaxic and olfactory behaviour. Temporal, topographical and kinematic reconstructions of homing behaviour, however, indicated that control rats, but not hippocampal rats, made direct high velocity return trips to the home base in both the light and the dark. Peak velocity of the trips occurred at the trip midpoint, independent of trip distance, suggesting the movements were preplanned. These results are discussed in relation to the ideas that dead reckoning is used in the homing of exploring rats and that this form of navigation involves the hippocampus.     

Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation.

Studies on foraging rats suggest that they can use visual, olfactory, and self-movement cues for spatial guidance, but their relative reliance on these different cues is not well understood. In the present study, rats left a hidden refuge to search for a large food pellet located somewhere on a circular table, and the accuracy with which they returned to the refuge with the food pellet was measured. Cue use was manipulated by administering probe trials from novel locations, blindfolding, moving the home cage relative to the table, rotating the table and using combinations of these manipulations. When visual cues were available and a consistent starting location used, a visual strategy dominated performance. When blindfolded, the rats used olfactory cues from the surface of the table and from the starting hole. When olfactory stimuli were made uninformative, by changing the starting hole and rotating the table, the rats still homed accurately, suggesting they used self-movement cues. In a number of cue combinations, in which cues gave conflicting information, performance degraded. The results suggest that rats display a hierarchical preference in using visual, olfactory and self-movement cues while at the same time being able to reaffirm or switch between various cue combinations. The results are discussed in relation to ideas concerning the neural basis of spatial navigation.     

Do rats with retrosplenial cortex lesions lack direction?

The retrosplenial cortex is seen as a convergence point for different classes of spatial cue, yet aside from allocentric processing, little is known about other cue types that depend on the integrity of this area. Rats with bilateral retrosplenial cortex lesions were, therefore, trained on a sequence of reinforced spatial alternation tasks designed to isolate different spatial strategies. Using a standard T-maze alternation procedure, which could be solved using multiple strategies, only a marginal lesion effect was observed. Next, by using two T-mazes set side-by-side in the light, and then the dark, it was possible to examine alternation around a fixed bearing (direction alternation). Retrosplenial cortex lesions only disrupted the latter (direction alternation) condition. Direction alternation is of particular interest as it presumably taxes head-direction information, and so provides a way of behaviourally assessing the contribution of this navigation system. Finally, rats were tested on a spatial working memory task in a radial-arm maze. A retrosplenial lesion deficit appeared when the maze was rotated mid-trial, as repeatedly found in previous studies. The pattern of findings in the present study strongly indicates that retrosplenial cortex lesions impair the use of direction cues for alternation, in addition to previously established impairments for allocentric-based navigation and path integration.     

Path integration following temporal lobectomy in humans

Path integration, a component of spatial navigation, is the process used to determine position information on the basis of information about distance and direction travelled derived from self-motion cues. Following on from studies in the animal literature that seem to support the role of the hippocampal formation in path integration, this facility was investigated in humans with focal brain lesions. Thirty-three neurosurgical patients (17 left temporal lobectomy, LTL; 16 right temporal lobectomy, RTL) and 16 controls were tested on a number of blindfolded tasks designed to investigate path integration and on a number of additional control tasks (assessing mental rotation and left-right orientation). In a test of the ability to compute a homing vector, the subjects had to return to the start after being led along a route consisting of two distances and one turn. Patients with RTL only were impaired at estimating the turn required to return to the start. On a second task, route reproduction was tested by requiring the subjects to reproduce a route consisting of two distances and one turn; the RTL group only were also impaired at reproducing the turn, but this impairment did not correlate with the homing vector deficit. There were no group differences on tasks where subjects were required to reproduce a single distance or a single turn. The results indicate that path integration is impaired in RTL patients only and suggest that the right temporal lobe plays a role in idiothetic spatial memory.     

Processing idiothetic cues to remember visited locations: hippocampal and vestibular contributions to radial-arm maze performance

This research examined whether rats can use idiothetic cues to form spatial memories in the radial-arm maze (RM) and whether the hippocampus is involved in such ability. A possible contribution of the vestibular system to RM performance was also investigated. Rats with excitotoxic hippocampal lesions and sham-operated controls were trained on two versions of the RM task. In the Light condition, a unique visual insert was apposed on each arm floor and rats could choose which arm to enter next by relying on visual and/or idiothetic stimuli. In the Dark condition, the task was administered in darkness and success required processing of idiothetic cues to remember visited locations on the maze. In experiment 1, the performance of lesioned rats was impaired in the Light condition, but both control and lesioned rats learned to avoid already visited arms. In the Dark condition, the performance of controls improved over time whereas a severe deficit was observed in rats with hippocampal lesions. Thus, control rats, but not hippocampal lesioned rats, can form spatial memories by processing idiothetic inputs. Experiment 2 showed that vestibular lesions disrupt performance in both the Light and the Dark conditions and confirmed that rats use idiothetic information, especially vestibular cues, while navigating in the RM. Therefore, cues generated during locomotion play an important role in hippocampal-dependent spatial memory.     

Effects of medial and dorsal cortex lesions on spatial memory in lizards

In mammals and birds, the hippocampus is a major learning and memory center that plays a prominent role in spatial memory, the use of distal cues to guide navigation. The role of reptilian hippocampal homologues, the medial and dorsal cortex, in spatial memory has not been thoroughly investigated. The medial and dorsal cortex of reptiles is known to play a role in learning both tasks that are hippocampally dependent and tasks that are not hippocampally dependent in mammals and birds. In order to examine the specific role of the medial and dorsal cortex in spatial memory, we trained medial cortex, dorsal cortex, and sham lesioned Cnemidophorus inornatus lizards to locate the one heated rock of four identical rocks spaced evenly around the perimeter of a circular, sand filled, arena in a cool room. We used probe trials to examine the strategies used by lizards to locate the goal. Medial cortex lesions and dorsal cortex lesions slowed acquisition and altered the strategies used to locate the goal. However, none of the lizards adopted a spatial strategy to locate the goal suggesting that the dorsal cortex and medial cortex are involved in using non-spatial strategies for navigation.     

Direction and distance deficits in path integration after unilateral vestibular loss depend on task complexity

The effects of peripheral vestibular disorders on the direction and distance components of the internal spatial representation were investigated. The ability of Menière's patients to perform path integration was assessed in different situations aimed at differentiating the level of spatial processing (simple versus complex tasks), the available sensory cues (proprioceptive, vestibular, or visual conditions), and the side of the path (towards the healthy versus the lesioned side). After exploring two legs of a triangle, participants were required either to reproduce the exploration path, to follow the reverse path, or to take a shortcut to the starting point of the path (triangle completion). Patients' performances were recorded before unilateral vestibular neurotomy (UVN) and during the time-course of recovery (1 week and 1 month) and were compared to those of matched control subjects tested at similar time intervals. Both the angular and linear path components of the trajectory were impaired for patients compared to controls. However, deficits were restricted to the complex tasks, which required a higher level of spatial processing. Most deficits were maximal 1 week after UVN, and some remained up to the first post-operative month. Spatial representation was differentially impaired according to the available sensory cues: deficits were absent in active locomotor blindfolded condition, appeared in conditions involving visual and vestibular information, and were maximal when visual cues alone were available. Finally, concerning the side of the path, unilateral vestibular loss led to global impairment of the internal spatial representation, yet some asymmetrical spatial performances were observed 1 week after UVN. On the whole, results suggest that the environment experienced by the patients is different after UVN and that a different internal spatial representation is constructed, especially for tasks requiring high levels of spatial processing.     

Navigation‐induced ZENK expression in the olfactory system of pigeons (Columba livia)

A large body of evidence indicates that pigeons use olfactory cues to navigate over unfamiliar areas with a differential contribution of the left and right hemispheres. In particular, the right nostril/olfactory bulb (OB) and left piriform cortex (Cpi) have been demonstrated to be crucially involved in navigation. In this study we analysed behaviour‐induced activation of the olfactory system, indicated by the expression of the immediate early gene ZENK, under different homing conditions. One experimental group was released from an unfamiliar site, the second group was transported to the unfamiliar site and back to the loft, and the third group was released in front of the loft. To evaluate the differential contribution of the left and/or right olfactory input, the nostrils of the pigeons were either occluded unilaterally or not. Released pigeons revealed the highest ZENK cell density in the OB and Cpi, indicating that the olfactory system is activated during navigation from an unfamiliar site. The groups with no plug showed the highest ZENK cell density, supporting the activation of the olfactory system probably being due to sensory input. Moreover, both Cpis seem to contribute differently to the navigation process. Only occlusion of the right OB resulted in a decreased ZENK cell expression in the Cpi, whereas occlusion of the left nostril had no effect. This is the first study to reveal neuronal activation patterns in the olfactory system during homing. Our data show that lateralized processing of olfactory cues is indeed involved in navigation over unfamiliar areas.