Distance and Location Cues in Retention of Movements by a Congenitally Blind Subject

Distinct computations are performed at multiple brain regions during the encoding of spatial environments. Neural representations in the hippocampal, entorhinal, and head direction (HD) networks during spatial navigation have been clearly documented, while the representational properties of the subicular complex (SC) are relatively underexplored, although it has extensive anatomic connections with various brain regions involved in spatial information processing. We simultaneously recorded single units from different subregions of the SC in male rats while they ran clockwise on a centrally placed textured circular track (four different textures, each covering a quadrant), surrounded by six distal cues. The neural activity was monitored in standard sessions by maintaining the same configuration between the cues, while in cue manipulation sessions, the distal and local cues were either rotated in opposite directions to create a mismatch between them or the distal cues were removed. We report a highly coherent neural representation of the environment and a robust coupling between the HD cells and the spatial cells in the SC, strikingly different from previous reports of coupling between cells from co-recorded sites. Neural representations were (1) originally governed by the distal cues under local-distal cue-conflict conditions, (2) controlled by the local cues in the absence of distal cues, and (3) governed by the cues that are perceived to be stable. We propose that such attractor-like dynamics in the SC might play a critical role in the orientation of spatial representations, thus providing a "reference map" of the environment for further processing by other networks.SIGNIFICANCE STATEMENT The subicular complex (SC) receives major inputs from the entorhinal cortex and the hippocampus, and head direction (HD) information directly from the HD system. Using cue-conflict experiments, we studied the hierarchical representation of the local and distal cues in the SC to understand its role in the cognitive map, and report a highly coherent neural representation with robust coupling between the HD cells and the spatial cells in different subregions of the SC exhibiting attractor-like dynamics unaffected by the cue manipulations, strikingly different from previous reports of coupling between cells from co-recorded sites. This unique feature may allow the SC to function as a single computational unit during the representation of space, which may serve as a reference map of the environment.

A number of computational models of hippocampal place cells incorporate attractor neural network architecture to simulate key findings in the place cell literature, including the properties of pattern completion, firing in the absence of visual input, and nonlinear responses to environmental manipulations. To test for evidence of attractor dynamics, ensembles of place cells were recorded using multiple-tetrode techniques. After many days of experience in an environment with salient local surface cues on a circular track and salient distal landmarks on the wall, the local surface cues were rotated as a set in opposition to the distal landmarks. The amount of mismatch between the local and distal sets of cues varied from 45 to 180°. If place cells were parts of strong attractors, then their place fields should follow either the local cues or the distal cues as an integrated ensemble. Instead, in single recording sessions, some place cells were controlled by the distal landmarks, other cells were controlled by the local cues, and other cells became silent or gained new fields. In some cases, individual place fields split in half, following both the local and distal cues. If place cells are indeed parts of attractor networks in the hippocampus, then the attractors may be weak relative to the inputs from external sources, such as representations of the sensory environment and representations of heading direction, in a familiar, well explored environment.

A number of computational models of hippocampal place cells incorporate attractor neural network architecture to simulate key findings in the place cell literature, including the properties of pattern completion, firing in the absence of visual input, and nonlinear responses to environmental manipulations. To test for evidence of attractor dynamics, ensembles of place cells were recorded using multiple-tetrode techniques. After many days of experience in an environment with salient local surface cues on a circular track and salient distal landmarks on the wall, the local surface cues were rotated as a set in opposition to the distal landmarks. The amount of mismatch between the local and distal sets of cues varied from 45 to 180 degrees. If place cells were parts of strong attractors, then their place fields should follow either the local cues or the distal cues as an integrated ensemble. Instead, in single recording sessions, some place cells were controlled by the distal landmarks, other cells were controlled by the local cues, and other cells became silent or gained new fields. In some cases, individual place fields split in half, following both the local and distal cues. If place cells are indeed parts of attractor networks in the hippocampus, then the attractors may be weak relative to the inputs from external sources, such as representations of the sensory environment and representations of heading direction, in a familiar, well explored environment.

This was a preliminary study of the effects of covert rehearsal, i.e., mental practice, on retention of movement in motor long-term memory. Rehearsal has been recognized as one of the most important factors in experiments on human memory ( 1 ) . There have been many studies of rehearsal in motor short-term memory (2), however, most studies of motor long-term memory concerning the role of covert rehearsal have been atheoretical (3). If rehearsal is necessary for retention beyond the typical short-term memory period of a few minutes, it follows that preventing rehearsal should produce poorer retention of movement information than conditions in which rehearsal is allowed. In the present study 18 right-handed subjects participated in a study of a linear positioning task. In the first phase three movement lengths, 10, 15, 25 cm, were used. A movement length was assigned to one of three rehearsal conditions: immediate recall, recall after 20 sec. of rehearsal, recall after 20 sec. interpolated activity (backward counting by threes). Rehearsal intervals were counterbalanced between subjects, and subjects received both distance and location information cues. For each trial subjects moved the slide carriage from right to left until a stop was reached. Following the appropriate rehearsal interval the stop was removed and the subject attempted to reproduce the movement three times. This procedure was followed for all three rehearsal intervals. Following the completion of this phase subjects received a word-analogy test. After a 10-min. period subjects received a surprise recall test, in which they attempted to reproduce each movement three times in the same serial order as presented in the initial phase. Movement error was recorded in centimeters. Since the movement lengths were used simply to provide a repertoire of movements to remember, errors were collapsed over movement lengths. Errors were also collapsed over reproduction attempts within rehearsal condirions. Analysis of absolute error2 indicated there was no significant effect for rehearsal condirions in the initial phase. However, there was a significant effect for rehearsal in the second phase (F = 4.04, p < .05). The cell means were 4.5, 2.8, 4.9 cm for 0, 20, and 20 sec. filled, respectively. Subsequent analysis (Tukey HSD = 1.9) indicated a significant difference between 20 sec. filled and 20 sec. rehearsal but not between 0-sec. and 20-sec. rehearsal groups. The separate analysis was performed for each phase because recall in the first phase is sequential whereas recall in the second phase is serial. These findings provide preliminary evidence that covert rehearsal increases the retention of movement in motor long-term memory. The rehearsal condition (20 sec.) led to superlor retention of movement compared to the noor block-rehearsal conditions. The data suggest study of rehearsal in motor long-term memory is warranted.

The effects of synchrony on spatial cue choice in a virtual wayfinding task

We developed a parallel computational model of a network of entorhinal and hippocampal cells influenced by synaptic plasticity to examine the stability of CA3 place fields under graded environmental perturbations. Place cells form single firing fields within an environment and are located in the CA1 and CA3 subregions of the hippocampus. They receive the majority of their spatial input from grid cells, which are located in the medial entorhinal cortex (MEC) and fire in hexagonal patterns within an environment [1]. We designed the model in the context of the “double rotation” experiment in which a rat circles a track with various local and distal cues that are rotated in opposite directions. In response to this rotation, some CA1 cells follow local cues, some follow distal cues, and some remap. In contrast, CA3 place fields are more coherently dominated by local cues [2]. This CA3 response is puzzling given that grid cells are more strongly controlled by distal cues [3]. Because local cues were rotated in a direction opposite to the rat’s movement, the backward shift of place fields [4] may affect the CA3 response. Cells in the lateral entorhinal cortex (LEC) show a slight tendency to follow local cues [3], and we used the model to investigate whether the backward shift couples with weak LEC input to cause CA3 cells to rotate with the local cues. In the model the MEC contains grid cells, and LEC cells are weakly tuned to local cues. CA1 and CA3 cells are governed by the integrate and fire model, which provides no bias for spiking at one location over another. Rate-based plasticity [5] applied to the connections from grid cells to hippocampal cells enables place fields to form, and spike-timing-dependent plasticity [6] applied to the connections among CA3 cells enables place fields to shift backward, as seen experimentally. We implemented the model in PETSc (Portable, Extensible Toolkit for Scientific Computation), a suite of data structures and routines for parallel computation. This implementation greatly increased both the number of tractable variables and the speed of computation. We simulated networks of up to 20,000 cells, and the computational time reduces by a factor of 15 as we move from one processor to 64 processors. Because the model is efficient, modular, and capable of simulating large networks, it is an efficient tool for examining the effect of synaptic plasticity on place field dynamics.

Spatial radial maze procedures and setups to dissociate local and distal relational spatial frameworks in humans

Animals can navigate an environment relying on different sources of information, such as geometrical or featural cues. The favoring of one type of information over another depends on multiple factors, such as inter-individual differences in behavior and cognition. Free-range chickens present different range use patterns, which may be explained by behavioral and cognitive differences. However, how behavior, cognition, and range use intercorrelate is still poorly understood. In this work, we aimed to further understand possible differences in behavior and cognition between two groups of free-range broiler chickens: those who frequently explore their range ('high rangers') and those who prefer to stay in or near the barn ('low rangers'). Prior to range access, individual behavior was measured in open field-, emergence-, and social motivation tests. To investigate cognitive differences, we analyzed whether exploratory behavior was linked to different performances in the use of distal and local spatial cues during an orientation task. During the social motivation test, low rangers showed a higher inclination to be near conspecifics than did high rangers. Our orientation tests show that chickens preferred to orientate themselves using the local cues over the distal cues. Individual differences were only found for distal, but not for local, cue use suggesting that demanding tasks are more efficient in revealing individual cognitive differences. Our results suggest that considering variation in social motivation may allow a more comprehensive understanding of chicken range use. Our results also support the importance of incorporating multiple aspects of individual differences to understand individual reactions to its environment.

Hippocampal place fields were recorded as rats explored a four-arm radial maze surrounded by curtains holding distal stimuli and with distinct local tactile, olfactory, and visual cues covering each arm. Systematic manipulations of the individual cues and their interrelationships showed that different hippocampal neurons encoded individual local and distal cues, relationships among cues within a stimulus set, and the relationship between the local and distal cues. Double rotation trials, which maintained stimulus relationships within distal and local cue sets, but altered the relationship between them, often changed the responses of the sampled neural population and produced new representations. After repeated double rotation trials, the incidence of new representations increased, and the likelihood of a simple rotation with one of the cue sets diminished. Cue scrambling trials, which altered the topological relationship within the local or distal stimulus set, showed that the cells that followed one set of controlled stimuli responded as often to a single cue as to the constellation. These cells followed the single cue when the stimulus constellation was scrambled, but often continued firing in the same place when the stimulus was removed or switched to respond to other cues. When the maze was surrounded by a new stimulus configuration, all of the cells either developed new place fields or stopped firing, showing that the controlled stimuli had persistent and profound influence over hippocampal neurons. Together, the results show that hippocampal neurons encode a hierarchical representation of environmental information.

The dentate gyrus is essential for remembering the fine details of experiences that comprise episodic memory. Dentate gyrus granule cells receive highly-processed sensory information and are hypothesized to perform a pattern separation function, whereby similar sensory inputs are transformed into orthogonal neural representations. Behaviorally, this is believed to enable distinct memory for highly interfering stimuli. Since the dentate gyrus is comprised of a large number of adult-born neurons, which have unique synaptic wiring and neurophysiological firing patterns, it has been proposed that neurogenesis may contribute to this process in unique ways. Some behavioral evidence exists to support this role, whereby neurogenesis-deficient rodents are impaired at discriminating the fine visuospatial details of experiences. However, the extent to which newborn neurons contribute to dentate gyrus-dependent learning tasks is unclear. Furthermore, since most studies of dentate gyrus function are conducted in male rats, little is known about how females perform in similar situations, and whether there might be sex differences in the function of adult neurogenesis. To address these issues, we examined spatial discrimination memory in transgenic male and female rats that lacked adult neurogenesis. The first task probed memory for the position of local objects in an open field, assessed by behavioral responses to novel object locations. The second task examined memory for distal environmental cues. All rats were able to successfully discriminate local and distal cue changes. Males and females also performed comparably, although females displayed higher levels of rearing and locomotion. Collectively, our results indicate that rats are capable of learning about local and distal cues in the absence of adult neurogenesis.

The extent to which small ensembles of neighboring hippocampal neurons alter their spatial firing patterns concurrently in response to stimulus manipulations was examined in young adult rats as well as in aged rats with and without memory impairment. Recordings from CA1 and CA3 cells were taken as rats performed a spatial radial-maze task that employed prominent distal visual stimuli attached to dark curtains surrounding the maze and local cues on each maze arm provided by inserts with distinctive visual, tactile, and olfactory stimuli. To test the influence of the different stimulus subsets, the distal and local cues were rotated 90 degrees in opposite directions (a Double Rotation). In response to this manipulation, place fields could maintain a fixed position to room coordinates, rotate with either the local or the distal cues, disappear, or new fields could appear. On average 79% of the cells within an ensemble responded in the same way, but only 37% of all ensembles were fully concordant. Typically discordant ensembles had place fields that rotated with one set of cues, whereas the other fields disappeared or new fields appeared. Ensembles in which the place fields rotated in two opposite directions were less frequent in young rats than would be expected by the occurrence of the individual responses, indicating selective competition between directly conflicting representations and ultimate suppression of one. These findings indicate that hippocampal neurons independently encode distinct subsets of the cues in a complex environment, although processing within the hippocampal network may actively reduce the simultaneous representation of conflicting orientation information. This kind of population activity might reflect the higher-order organization of new memories within an established knowledge framework or schema. Concordance was higher in aged memory-impaired rats than in young rats, and the suppression of conflicting representations was absent in these rats. These findings suggest that age-related memory impairment is at least in part associated with a decrease in the scope of information coded and in the coordination of encoded representations.

Human navigation studies show that landmarks are used for orientation, whereas objects contribute to the contextual representation of an environment. What constitutes a landmark? Classic rodent studies show that hippocampal place fields are controlled by distal, polarizing cues. Place fields, however, are also influenced by local cues. One difficulty in examining mechanisms by which distal and local cues influence the activity of hippocampal cells is that distant cues are necessarily processed visually, whereas local cues are generally multimodal. Here, we compared the effects of 90° rotations under different cue conditions in which cues were restricted to the visual modality. Three two-dimensional visual cue conditions were presented in a square open field: a large vertical cue on one wall, a large floor cue in a corner abutting two walls, and a smaller complex floor cue in a corner adjacent to two walls. We show that rotations of large distal cues, whether on the wall or floor, were equally effective in controlling place fields. Rotations of the smaller floor cues were significantly more likely to result in remapping, whether or not animals were also exposed to the distal polarizing cues. Responses of distal and local cues were affected differently by extended experience. Our data provide evidence that hippocampal place cell responses to visual cues are influenced by perspective, salience of the cue, and prior experience. The hippocampus processes visual cues either as stable landmarks useful for orientation and navigation or as nonstationary objects or features of the local environment available for associative learning or binding items in context.

The observation of hippocampal place cells forms a major line of evidence supporting the view that the hippocampus is dedicated to spatial processing. However, most studies demonstrating the spatial properties of hippocampal unit activity have employed tasks that emphasize spatial cues but minimize nonspatial cues. In the present experiment we recorded the activity of hippocampal complex-spike cells from rats performing a nonspatial radial maze task. Performance in this task was guided by local visual-tactile cues on the maze arms, while distal spatial cues were minimized and made irrelevant. The influence of three variables on unit activity was examined:type of cue on an arm, spatial location of an arm, and the relative position of the animal on an arm. Of the units recorded, almost one-fifth were classified as "cue cells" in that their activity was associated with cue type but not spatial location. Conversely, a similar proportion of the units were classified as "place cells" in that their activity was associated with location, but not cue type. In an additional similar proportion of units, firing was influenced only by relative position and not by local cues or spatial locations. For the majority of units, however, firing was related to combinations of these three variables, indicating that most hippocampal neurons encoded conjunctions or relations between spatial and local cue information. This pattern of results indicates that when local rather than distal spatial cues are emphasized, hippocampal neural activity is strongly influenced by salient nonspatial cues and shows no overwhelming predominance of place coding. These findings are at odds with the hypothesis that the hippocampus is selectively involved in spatial processing and, conversely, support the broader view that the hippocampus encodes both spatial and nonspatial relations among important experimental variables.

To isolate location and distance cues a two-dimensional movement task was given to 32 college students. Reliability of location cues was varied; a criterion distance was recalled accurately with and without location cues.

Although there is evidence to suggest that animal domestication acts as a modulator of spatial orientation, little is known on how domesticated animals, compared to their wild counterparts, orientate themselves when confronted to different environmental cues. Here, using domesticated White Leghorn chicks, and their ancestor, the Red Junglefowl (Gallus gallus), our main objective was to investigate how bird domestication influences the use of distal and local cues, during an orientation task. We also investigated the memory retention of these cues over time, and how persistent/flexible individuals from both breeds were at pecking at unreachable mealworms. Our results showed that the breeds did not differ in their use of distal or local cues, with both showing a marked preference for the use of local cues over distal ones. Over time, individual performance declined, but this was not influenced by the type of cue present during the tests, nor by the breed. Domesticated chicks showed greater signs of persistency compared to their wild conspecifics. In conclusion, domestication did not seem to alter how birds orientate spatially, but may have caused more subtle changes, such as an increase in behavioral persistency, a feature that may be adaptative in human-controlled and homogenous environments.