Calibrating space: exploration is important for allothetic and idiothetic navigation

Allothetic and idiothetic navigation strategies rely on very different cues and computational procedures. Allothetic navigation uses the relationships between external cues (visual, auditory, and olfactory) and mapping or geometrical calculations to locate places. Idiothetic navigation relies on cues generated by self-movement (proprioceptive cues or cues from optic, auditory, and olfactory flow, or efference copy of motor commands) and path integration to locate a present location and/or a starting point. Whereas it is theorized that exploratory behavior is used by animals to create a central representation of allothetic cues, it is unclear whether exploration plays a role in idiothetic navigation. Computational models suggest that either a reference frame, calibrated by exploration, or vector addition, without reference to exploration, could support path integration. The present study evaluated the contribution of exploration in these navigation strategies by comparing its contribution to the solution of both allothetic and idiothetic navigation problems. In two experiments, rats were trained to forage on an open table for large food pellets, which they then carried to a refuge to eat. Once trained, they were given probe trials from novel locations in either normal light, which permits the use of allothetic cues, or in infrared light, which requires the use of idiothetic cues. When faced with a new problem in either lighting condition, the rats first explored the foraging table before navigating directly home with the food. That exploration is equally important for allothetic and idiothetic navigation, suggests that both navigation strategies require a calibrated representation of the environment.     

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.     

Contributions of cingulate cortex to two forms of spatial learning and memory

The contribution of anterior and posterior cingulate cortical areas to spatial learning and memory was examined in 4 experiments using the place-navigation task. Rats with complete bilateral cingulate cortex aspiration or aspiration of posterior cingulate cortex (area 29) alone could not swim directly to a hidden platform located in a fixed place. When animals with these lesions were tested for 40 d in a place-alternation task in which they received 16 daily trials with the platform placed in a new location each day, they did not show reliable improvement in place navigation. The inability to swim to changing locations or to a single location was not overcome by preoperative training in these tasks. Rats with anterior cingulate cortex aspirations showed a less severe impairment in both tasks and, with more training than is necessary for control rats, they acquired near-normal place-navigation accuracy. Rats with complete cingulate cortex aspiration were almost as accurate as control rats in learning to swim to a visible platform. The results imply that posterior cingulate areas play an essential role in the use of topographical information, probably by transmitting and elaborating information passing between the hippocampal system and neocortical association areas.     

Does the cingulate cortex contribute to spatial conditional associative learning in the rat?

Rats with lesions to the anterior or posterior (retrosplenial) region of the cingulate cortex and rats with lesions that included both the anterior and posterior cingulate cortex were tested on a visual–spatial conditional task in which they had to learn to approach one of the two objects depending on the spatial context within which they were embedded. Lesions restricted to either the anterior or the retrosplenial cingulate region did not impair learning of this task which is known to be very sensitive to the effects of hippocampal lesions. Complete lesions of the cingulate cortex gave rise to only a minor retardation in learning. In contrast, lesions to the retrosplenial cortex impaired performance on a spatial navigation task and the classic radial maze. These results suggest that the retrosplenial portion of the cingulate region forms part of a hippocampal circuit underlying learning about spatial responses. The dissociation between the effects of lesions of the cingulate region on different classes of behavior known to be associated with hippocampal function suggests that, although this neural structure does play a role in an extended hippocampal circuit underlying spatial learning, its role in such learning may be a selective one. © 2009 Wiley‐Liss, Inc.     

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.     

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.     

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.     

Behavioural and anatomical studies of the posterior parietal cortex in the rat

Primates have an area of posterior cortex characterized by multimodal sensory projections to and from the frontal association cortex and a clear behavioural syndrome resulting from lesions to this zone. The posterior association cortex of the rat was examined in two series of experiments, one anatomical and one behavioural, to see if an analogous region could be found. The anatomical connections of Krieg's area 7 in the rat were examined by placing the retrograde tracer, True blue, into the frontal or posterior cortex, and the behaviour of rats with this cortex removed was studied on a variety of tasks. This area appears to be a multimodal sensory association region. It receives projections from striate (area 17), extrastriate (areas 18a and 18b), and somatosensory cortex (area 3). It is also reciprocally connected with the posterior cingulate cortex and two frontal association zones in the medial frontal cortex, namely the anterior cingulate cortex and the frontal eye fields. Lesions produced deficits on tasks of tactile discrimination, and walking a narrow beam, two tasks requiring animals to navigate accurately to a point in space, and a task requiring the association of two spatially discontiguous cues. The animals were not impaired at navigating to a cue or in opening puzzle latches. Overall, the results show that the rat has a sensory association zone that may be analogous to the posterior parietal cortex of primates.     

The role of the prefrontal cortex in object-place learning: a test of the attribute specificity model

In order to test an attribute specificity model of prefrontal cortex function, rats with lesions in the prelimbic-infralimbic (PL-IL) or anterior cingulate and precentral (AC-PC) subregions of the medial prefrontal cortex and controls were trained on an object-place paired associate task. Rats with AC-PC lesions acquired the task as readily as controls. In contrast, the PL-IL lesioned rats did not learn the task. Whenever higher order processing is required to solve a task, the data support an attribute-specificity model of prefrontal cortex function in that the PL-IL cortices support both object and place attribute information in a variety of tasks including object-place paired associate learning.     

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.     

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.     

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.     

Comparing the effects of selective cingulate cortex lesions and cingulum bundle lesions on water maze performance by rats

The ability of rats to learn the location of a hidden platform in a swim maze was compared in animals with excitotoxic lesions of the anterior or posterior (retrosplenial) cingulate cortex or radiofrequency lesions of the cingulum bundle or fimbria-fornix. Performance of this allocentric spatial task was unaffected by the posterior cingulate cortex lesions, while anterior cingulate cortex damage produced only a mild acquisition deficit. Transection of the fornix and lesions of the cingulum bundle produced similar patterns of impairment on initial acquisition, but the cingulum bundle lesions had less effect on reversal of the task. The results from the water maze, and from a subsequent T-maze alternation task, indicate that cingulum bundle lesions can produce a spatial deficit that is similar, but milder, to that observed after fornix transection. The results of the excitotoxic lesions suggest that previous studies examining conventional cingulate lesions may have been influenced by damage to adjacent fibre tracts, such as the cingulum bundle.     

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.     

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.     

Impairment and recovery on a food foraging task following unilateral vestibular deafferentation in rats

It has been suggested that the vestibular system may contribute to the development of higher cognitive function, especially spatial learning and memory that uses idiothetic cues (e.g., dead reckoning). However, few studies have been done using behavioral tasks that could potentially separate the animals' ability for dead reckoning from piloting. The food foraging task requires the animal to continuously monitor and integrate self-movement cues and generate an accurate return path. It has been shown that bilateral vestibular-lesioned rats were impaired on this task. The present study used the same task to further examine the contribution of vestibular information to spatial navigation by comparing unilateral and bilateral lesions and by testing the animals at different time points following the lesion. The results demonstrated that animals with unilateral vestibular deafferentation were impaired in performing the task in the dark at 3 months after the lesion, and this impairment disappeared at 6 months after the lesion. This supports the notion that vestibular information contributes to dead reckoning and suggests possible recovery of function over time after the lesion. Animals with bilateral vestibular deafferentation were not able to be tested on the foraging task because they exhibited behavior distinct from the unilateral-lesioned animals, with significant hesitation in leaving their home cage for as long as 6 months after the lesion.     

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.     

Dissociable roles of the medial prefrontal cortex, the anterior cingulate cortex, and the hippocampus in behavioural flexibility revealed by serial reversal of three-choice discrimination in rats

Contributions of different limbic cortical areas to mediation of behavioural flexibility were examined using repeated acquisition of three-choice discrimination in operant chambers. Rats were trained on a series of positional discrimination tasks with three levers, where position of the correct lever remained the same within a task but shifted across tasks. Ibotenic acid lesions of the medial prefrontal cortex impaired acquisition of each discrimination task by increasing errors specifically in the early phase of each task. These errors were characterised by perseveration to the previously correct lever. By contrast, lesions of the anterior cingulate cortex resulted in the impairment of discrimination in general without inducing perseveration; the impairment was instead characterised by disruption of general error-correction processes. Hippocampal lesions severely impaired learning by increasing perseverative tendencies that were present throughout the learning stages in each task. These results extend our understanding of the contributions of the different nodes of the limbic cortico-striatal circuit to different aspects of behavioural flexibility.     

Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis

The role of forebrain cholinergic projections in place navigation learning was assessed in two experiments. Following surgery, rats were required to learn the spatial location of an underwater platform on the basis of distal room cues. Bilateral injections of ibotenic acid into the nucleus basalis magnocellularis depleted choline acetyltransferase (ChAT) from the anterior and temporoparietal cortex but not the hippocampus. Separate histological studies confirmed the accuracy of the lesions and demonstrated a marked loss of cortical acetylcholinesterase. These rats subsequently showed no deficits in spatial learning or memory. In a second experiment, bilateral lesions of the vertical limb of the diagonal band of Broca and medial septum depleted ChAT from the hippocampus and posterior cortex but not the anterior cortex. Histological studies confirmed the accuracy of the lesion and showed a pronounced loss of acetylcholinesterase from the hippocampus. These rats were deficient in spatial learning and showed reduced spatial bias during transfer tests. The data are discussed in the light of the hypothesis that the cholinergic innervation of the hippocampus plays a key role in spatial reference memory processes involved in place navigation.