The well-worn route revisited: Striatal and hippocampal system contributions to familiar route navigation.

Classic research has shown a division in the neuroanatomical structures that support flexible (e.g., short-cutting) and habitual (e.g., familiar route following) navigational behavior, with hippocampal-caudate systems associated with the former and putamen systems with the latter. There is, however, disagreement about whether the neural structures involved in navigation process particular forms of spatial information, such as associations between constellations of cues forming a cognitive map, versus single landmark-action associations, or alternatively, perform particular reinforcement learning algorithms that allow the use of different spatial strategies, so-called model-based (flexible) or model-free (habitual) forms of learning. We sought to test these theories by asking participants (N = 24) to navigate within a virtual environment through a previously learned, 9-junction route with distinctive landmarks at each junction while undergoing functional magnetic resonance imaging (fMRI). In a series of probe trials, we distinguished knowledge of individual landmark-action associations along the route versus knowledge of the correct sequence of landmark-action associations, either by having absent landmarks, or "out-of-sequence" landmarks. Under a map-based perspective, sequence knowledge would not require hippocampal systems, because there are no constellations of cues available for cognitive map formation. Within a learning-based model, however, responding based on knowledge of sequence would require hippocampal systems because prior context has to be utilized. We found that hippocampal-caudate systems were more active in probes requiring sequence knowledge, supporting the learning-based model. However, we also found greater putamen activation in probes where navigation based purely on sequence memory could be planned, supporting models of putamen function that emphasize its role in action sequencing.

Precision in spatial working memory examined with mouse pointing.

The capacity of visuospatial working memory (VSWM) is limited. However, there is continued debate surrounding the nature of this capacity limitation. The resource model (Bays et al., 2009) proposes that VSWM capacity is limited by the precision with which visuospatial features can be retained. In one of the few studies of spatial working memory, Schneegans and Bays (2016) report that memory guided pointing responses show a monotonic decrease in precision as set size increases, consistent with resource models. Here we report two conceptual replications of this study that use mouse responses rather than pointing responses. Overall results are consistent with the resource model, as there was an exponential increase in localisation error and monotonic increases in the probability of misbinding and guessing with increases in set size. However, an unexpected result of Experiment One was that, unlike Schneegans and Bays (2016), imprecision did not increase between set sizes of 2 and 8. Experiment Two replicated this effect and ruled out the possibility that the invariance of imprecision at set sizes greater than 2 was a product of oculomotor strategies during recall. We speculate that differences in imprecision are related to additional visuomotor transformations required for memory-guided mouse localisation compared to memory-guided manual pointing localisation. These data demonstrate the importance of considering the nature of the response modality when interpreting VSWM data.

Dynamic resource allocation in spatial working memory during full and partial report tasks.

Serial position effects are well-documented in working memory literature. Studies of spatial short-term memory that rely on binary response; full report tasks tend to report stronger primacy than recency effects. In contrast, studies that utilize a continuous response, partial report task report stronger recency than primacy effects (Gorgoraptis, Catalao, Bays, & Husain, 2011; Zokaei, Gorgoraptis, Bahrami, Bays, & Husain, 2011). The current study explored the idea that probing spatial working memory using full and partial continuous response tasks would produce different distributions of visuospatial working memory resources across spatial sequences and, therefore, explain the conflicting results in the literature. Experiment 1 demonstrated that primacy effects were observed when memory was probed with a full report task. Experiment 2 confirmed this finding while controlling eye movements. Critically, Experiment 3 demonstrated that switching from a full to a partial report task abolished the primacy effect and produced a recency effect, consistent with the idea that the distribution of resources in visuospatial working memory depends on the type of recall required. It is argued that the primacy effect in the whole report task arose from the accumulation of noise caused by the execution of multiple spatially directed actions during recall, whereas the recency effect in the partial report task reflects the redistribution of preallocated resources when an anticipated item is not presented. These data show that it is possible to reconcile apparently contradictory findings within the resource theory of spatial working memory and the importance of considering how memory is probed when interpreting behavioral data through the lens of resource theories of spatial working memory.

Oculomotor rehearsal in visuospatial working memory.

The neural and cognitive mechanisms of spatial working memory are tightly coupled with the systems that control eye movements, but the precise nature of this coupling is not well understood. It has been argued that the oculomotor system is selectively involved in rehearsal of spatial but not visual material in visuospatial working memory. However, few studies have directly compared the effect of saccadic interference on visual and spatial memory, and there is little consensus on how the underlying working memory representation is affected by saccadic interference. In this study we aimed to examine how working memory for visual and spatial features is affected by overt and covert attentional interference across two experiments. Participants were shown a memory array, then asked to either maintain fixation or to overtly or covertly shift attention in a detection task during the delay period. Using the continuous report task we directly examined the precision of visual and spatial working memory representations and fit psychophysical functions to investigate the sources of recall error associated with different types of interference. These data were interpreted in terms of embodied theories of attention and memory and provide new insights into the nature of the interactions between cognitive and motor systems.

The spatial layout of doorways and environmental boundaries shape the content of event memories.

Physical boundaries in our environment have been observed to define separate events in episodic memory. To date, however, there is little evidence that the spatial properties of boundaries exert any control over event memories. To examine this possibility, we conducted four experiments that took manipulations involving boundaries that have been demonstrated to influence spatial representations, and adapted them for use in an episodic object memory paradigm. Here, participants were given 15 min to freely explore an environment that contained 36 objects, equally dispersed among six discriminable buildings. In a subsequent test of object-location binding, participants were required to indicate where they remembered encountering the objects. In Experiment 1 the spatial properties of the building boundaries were identical; however, in Experiment 2 the boundaries were differentiated by their geometric shape and the location of the doorways in the buildings. In the test phases of these experiments, we observed a shift from a bias towards remembering the positions of objects within a building but not the building itself (Experiment 1), to a bias towards remembering which building an object was in but not the location within the building (Experiment 2). In Experiment 3, the buildings shared the same geometry but were differentiated by the locations of doorways, and we observed no significant differences between response types. Finally, in Experiment 4, the buildings were uniquely shaped but shared the same doorway location, and we observed a bias towards remembering the positions of objects within a building. In addition, exploratory analyses of non-spatial interference revealed more correct recall for objects housed in the first building a participant visited during exploration, compared to all other buildings. Together, our data indicates that the location of doorways in boundaries and, to a lesser extent, boundary geometries influence event models, and that a primacy effect can be observed in the recall of multiple object-location bindings.

Frequency matters: how changes in hippocampal theta frequency can influence temporal coding, anxiety-reduction, and memory.

Hippocampal theta frequency is a somewhat neglected topic relative to theta power, phase, coherence, and cross-frequency coupling. Accordingly, here we review and present new data on variation in hippocampal theta frequency, focusing on functional associations (temporal coding, anxiety reduction, learning, and memory). Taking the rodent hippocampal theta frequency to running-speed relationship as a model, we identify two doubly-dissociable frequency components: (a) the slope component of the theta frequency-to-stimulus-rate relationship ("theta slope"); and (b) its y-intercept frequency ("theta intercept"). We identify three tonic determinants of hippocampal theta frequency. (1) Hotter temperatures increase theta frequency, potentially consistent with time intervals being judged as shorter when hot. Initial evidence suggests this occurs via the "theta slope" component. (2) Anxiolytic drugs with widely-different post-synaptic and pre-synaptic primary targets share the effect of reducing the "theta intercept" component, supporting notions of a final common pathway in anxiety reduction involving the hippocampus. (3) Novelty reliably decreases, and familiarity increases, theta frequency, acting upon the "theta slope" component. The reliability of this latter finding, and the special status of novelty for learning, prompts us to propose a Novelty Elicits Slowing of Theta frequency (NEST) hypothesis, involving the following elements: (1) Theta frequency slowing in the hippocampal formation is a generalised response to novelty of different types and modalities; (2) Novelty-elicited theta slowing is a hippocampal-formation-wide adaptive response functioning to accommodate the additional need for learning entailed by novelty; (3) Lengthening the theta cycle enhances associativity; (4) Even part-cycle lengthening may boost associativity; and (5) Artificial theta stimulation aimed at enhancing learning should employ low-end theta frequencies.

The effects of spatial stability and cue type on spatial learning: Implications for theories of parallel memory systems.

Some theories of spatial learning predict that associative rules apply under only limited circumstances. For example, learning based on a boundary has been claimed to be immune to cue competition effects because boundary information is the basis for the formation of a cognitive map, whilst landmark learning does not involve cognitive mapping. This is referred to as the cue type hypothesis. However, it has also been claimed that cue stability is a prerequisite for the formation of a cognitive map, meaning that whichever cue type was perceived as stable would enter a cognitive map and thus be immune to cue competition, while unstable cues will be subject to cue competition, regardless of cue type. In experiments 1 and 2 we manipulated the stability of boundary and landmark cues when learning the location of two hidden goals. One goal location was constant with respect to the boundary, and the other constant with respect to the landmark cues. For both cue types, the presence of distal orientation cues provided directional information. For half the participants the landmark cues were unstable relative to the boundary and orientation cues, whereas for the remainder of the participants the boundary was unstable relative to landmarks and orientation cues. In a second stage of training, all cues remained stable so that both goal locations could be learned with respect to both landmark and boundary information. According to the cue type hypothesis, boundary information should block learning about landmarks regardless of cue stability. According to the cue stability hypothesis, however, landmarks should block learning about the boundary when the landmarks appear stable relative to the boundary. Regardless of cue type or stability the results showed reciprocal blocking, contrary to both formulations of incidental cognitive mapping. Experiment 3 established that the results of Experiments 1 and 2 could not be explained in terms of difficulty in learning certain locations with respect to different cue types. In a final experiment, following training in which both landmarks and boundary cues signalled two goal locations, a new goal location was established with respect to the landmark cues, before testing with the boundary, which had never been used to define the new goal location. The results of this novel test of the interaction between boundary and landmark cues indicated that new learning with respect to the landmark had a profound effect on navigation with respect to the boundary, counter to the predictions of incidental cognitive mapping of boundaries.

Uncertainty and predictiveness modulate attention in human predictive learning.

[Correction Notice: An Erratum for this article was reported online in Journal of Experimental Psychology: General on Jan 14 2021 (see record 2021-07705-001). In the article, formatting for UK Research Councils funding was omitted. The author note and copyright line now reflect the standard acknowledgment of and formatting for the funding received for this article. All versions of this article have been corrected.] Attention determines which cues receive processing and are learned about. Learning, however, leads to attentional biases. In the study of animal learning, in some circumstances, cues that have been previously predictive of their consequences are subsequently learned about more than are nonpredictive cues, suggesting that they receive more attention. In other circumstances, cues that have previously led to uncertain consequences are learned about more than are predictive cues. In human learning, there is a clear role for predictiveness, but a role for uncertainty has been less clear. Here, in a human learning task, we show that cues that led to uncertain outcomes were subsequently learned about more than were cues that were previously predictive of their outcomes. This effect occurred when there were few uncertain cues. When the number of uncertain cues was increased, attention switched to predictive cues. This pattern of results was found for cues (1) that were uncertain because they led to 2 different outcomes equally often in a nonpredictable manner and (2) that were used in a nonlinear discrimination and were not predictive individually but were predictive in combination with other cues. This suggests that both the opposing predictiveness and uncertainty effects were determined by the relationship between individual cues and outcomes rather than the predictive strength of combined cues. These results demonstrate that learning affects attention; however, the precise nature of the effect on attention depends on the level of task complexity, which reflects a potential switch between exploration and exploitation of cues. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Spontaneous object-location memory based on environmental geometry is impaired by both hippocampal and dorsolateral striatal lesions.

We examined the role of the hippocampus and the dorsolateral striatum in the representation of environmental geometry using a spontaneous object recognition procedure. Rats were placed in a kite-shaped arena and allowed to explore two distinctive objects in each of the right-angled corners. In a different room, rats were then placed into a rectangular arena with two identical copies of one of the two objects from the exploration phase, one in each of the two adjacent right-angled corners that were separated by a long wall. Time spent exploring these two objects was recorded as a measure of recognition memory. Since both objects were in different locations with respect to the room (different between exploration and test phases) and the global geometry (also different between exploration and test phases), differential exploration of the objects must be a result of initial habituation to the object relative to its local geometric context. The results indicated an impairment in processing the local geometric features of the environment for both hippocampus and dorsolateral striatum lesioned rats compared with sham-operated controls, though a control experiment showed these rats were unimpaired in a standard object recognition task. The dorsolateral striatum has previously been implicated in egocentric route-learning, but the results indicate an unexpected role for the dorsolateral striatum in processing the spatial layout of the environment. The results provide the first evidence that lesions to the hippocampus and dorsolateral striatum impair spontaneous encoding of local environmental geometric features.

Distinct and combined responses to environmental geometry and features in a working-memory reorientation task in rats and chicks.

The original provocative formulation of the 'geometric module' hypothesis was based on a working-memory task in rats which suggested that spontaneous reorientation behavior is based solely on the environmental geometry and is impervious to featural cues. Here, we retested that claim by returning to a spontaneous navigation task with rats and domestic chicks, using a single prominent featural cue (a striped wall) within a rectangular arena. Experiments 1 and 2 tested the influence of geometry and features separately. In Experiment 1, we found that both rats and chicks used environmental geometry to compute locations in a plain rectangular arena. In Experiment 2, while chicks failed to spontaneously use a striped wall in a square arena, rats showed a modest influence of the featural cue as a local marker to the goal. The critical third experiment tested the striped wall inside the rectangular arena. We found that although chicks solely relied on geometry, rats navigated based on both environmental geometry and the featural cue. While our findings with rats are contrary to classic claims of an impervious geometric module, they are consistent with the hypothesis that navigation by boundaries and features may involve distinct underlying cognitive computations. We conclude by discussing the similarities and differences in feature-use across tasks and species.

En route to delineating hippocampal roles in spatial learning.

The precise role played by the hippocampus in spatial learning tasks, such as the Morris Water Maze (MWM), is not fully understood. One theory is that the hippocampus is not required for 'knowing where' but rather is crucial in 'getting there'. To explore this idea in the MWM, we manipulated 'getting there' variables, such as passive transport or active swimming towards the hidden platform, in rats with and without hippocampal lesions. Our results suggested that for intact rats, self-motion cues enroute to the hidden goal were a necessary component for 'place learning' to progress. Specifically, intact rats could not learn the hidden goal location, when passively transported to it, despite extensive training. However, when rats were either given hippocampal lesions, or placed in a light-tight box during transportation to the hidden goal, passive-placement spatial learning was facilitated. In a subsequent experiment, the 'getting there' component of place navigation was simplified, via the placement of two overhead landmarks, one of which served as a beacon. When 'getting there' was made easier in this way, hippocampal lesions did not induce deficits in 'knowing where' the goal was. In fact, similar to the facilitation observed in passive-placement spatial learning, hippocampal lesions improved landmark learning relative to controls. Finally, demonstrating that our lesions were sufficiently deleterious, hippocampal-lesioned rats were impaired, as predicted, in an environmental-boundary based learning task. We interpret these results in terms of competition between multiple memory systems, and the importance of self-generated motion cues in hippocampal spatial mapping.

Walking through doorways differentially affects recall and familiarity.

Previous research has reported that walking through a doorway to a new location makes memory for objects and events experienced in the previous location less accurate. This effect, termed the location updating effect, has been used to suggest that location changes are used to mark boundaries between events in memory: memories for objects encountered within the current event are more available than those from beyond an event boundary. Within a computer-generated memory task, participants navigated through virtual rooms, walking through doorways, and interacting with objects. The accuracy and their subjective experience of their memory for the objects (remember/know and confidence) were assessed. The findings showed that shifts in location decreased accurate responses associated with the subjective experience of remembering but not those associated with the experience of knowing, even when considering only the most confident responses in each condition. These findings demonstrate that a shift in location selectively impacts recollection and so contributes to our understanding of boundaries in event memory.

The response strategy and the place strategy in a plus-maze have different sensitivities to devaluation of expected outcome.

Previous studies have suggested that spatial navigation can be achieved with at least two distinct learning processes, involving either cognitive map-like representations of the local environment, referred to as the "place strategy", or simple stimulus-response (S-R) associations, the "response strategy". A similar distinction between cognitive/behavioral processes has been made in the context of non-spatial, instrumental conditioning, with the definition of two processes concerning the sensitivity of a given behavior to the expected value of its outcome as well as to the response-outcome contingency ("goal-directed action" and "S-R habit"). Here we investigated whether these two versions of dichotomist definitions of learned behavior, one spatial and the other non-spatial, correspond to each other in a formal way. Specifically, we assessed the goal-directed nature of two navigational strategies, using a combination of an outcome devaluation procedure and a spatial probe trial frequently used to dissociate the two navigational strategies. In Experiment 1, rats trained in a dual-solution T-maze task were subjected to an extinction probe trial from the opposite start arm, with or without prefeeding-induced devaluation of the expected outcome. We found that a non-significant preference for the place strategy in the non-devalued condition was completely reversed after devaluation, such that significantly more animals displayed the use of the response strategy. The result suggests that the place strategy is sensitive to the expected value of the outcome, while the response strategy is not. In Experiment 2, rats with hippocampal lesions showed significant reliance on the response strategy, regardless of whether the expected outcome was devalued or not. The result thus offers further evidence that the response strategy conforms to the definition of an outcome-insensitive, habitual form of instrumental behavior. These results together attest a formal correspondence between two types of dual-process accounts of animal learning and behavior.

Dorsolateral striatal lesions impair navigation based on landmark-goal vectors but facilitate spatial learning based on a "cognitive map".

In three experiments, the nature of the interaction between multiple memory systems in rats solving a variation of a spatial task in the water maze was investigated. Throughout training rats were able to find a submerged platform at a fixed distance and direction from an intramaze landmark by learning a landmark-goal vector. Extramaze cues were also available for standard place learning, or "cognitive mapping," but these cues were valid only within each session, as the position of the platform moved around the pool between sessions together with the intramaze landmark. Animals could therefore learn the position of the platform by taking the consistent vector from the landmark across sessions or by rapidly encoding the new platform position on each session with reference to the extramaze cues. Excitotoxic lesions of the dorsolateral striatum impaired vector-based learning but facilitated cognitive map-based rapid place learning when the extramaze cues were relatively poor (Experiment 1) but not when they were more salient (Experiments 2 and 3). The way the lesion effects interacted with cue availability is consistent with the idea that the memory systems involved in the current navigation task are functionally cooperative yet associatively competitive in nature.

Revaluation of geometric cues reduces landmark discrimination via within-compound associations.

Rats were trained in a triangular water maze in which a compound of geometric and landmark cues indicated the position of a submerged platform. Rats that then underwent revaluation of the geometric cues in the absence of the landmarks subsequently failed to discriminate between the landmarks. In contrast, those animals that received geometry training consistent with their previous experience of the geometry-landmark compound continued to discriminate the landmark cues. The experiment showed that within-compound associations had formed between the geometry and landmarks, and that representations of absent geometric cues could be evoked via presentation of the landmark cues alone. We argue that these evoked representations of the absent geometry cues can counteract any overshadowing of the landmark by geometry cues, and may sometimes result in potentiation. The results of this study do not support theories of cue-competition failure based on independent cue processing, but remain readily explicable by appeal to an account based on within-compound associations.

Transfer of spatial search between environments in human adults and young children (Homo sapiens): implications for representation of local geometry by spatial systems.

Whether animals represent environmental geometry in a global and/or local way has been the subject of recent debate. We applied a transfer of search paradigm between rectangular- and kite-shaped arenas to examine the performance of human adults (using virtual environments) and children of 2.5-3.5 years (using real arenas). Adults showed robust transfer to a congruent corner in a kite-shaped arena, following training in a rectangular-shaped arena in two paradigms modeled on those used with rats and young children respectively. In contrast, the children showed no evidence of transfer of search, despite above chance performance in the rectangular arena, and above chance performance in a study where search occurred in the kite arena only. The pattern of findings suggests global aspects of environmental geometry may be used to re-establish heading, and that the matching of elements of local geometry in new global contexts may be an advanced developmental achievement.

Within-compound associations explain potentiation and failure to overshadow learning based on geometry by discrete landmarks.

In three experiments, rats were trained to locate a submerged platform in one of the base corners of a triangular arena above each of which was suspended one of two distinctive landmarks. In Experiment 1, it was established that these landmarks differed in their salience by the differential control they gained over behavior after training in compound with geometric cues. In Experiment 2, it was shown that locating the platform beneath the less salient landmark potentiated learning based on geometry compared with control rats for which landmarks provided ambiguous information about the location of the platform. The presence of the more salient landmark above the platform for another group of animals appeared to have no effect on learning based on geometry. Experiment 3 established that these landmark and geometry cues entered into within-compound associations during compound training. We argue that these within-compound associations can account for the potentiation seen in Experiment 2, as well as previous failures to demonstrate overshadowing of geometric cues. We also suggest that these within-compound associations need not be of different magnitudes, despite the different effects of each of the landmarks on learning based on geometry seen in Experiment 2. Instead, within-compound associations appear to mitigate the overshadowing effects that traditional theories of associative learning would predict.

Overshadowing of geometry learning by discrete landmarks in the water maze: effects of relative salience and relative validity of competing cues.

The effects of stimulus salience and cue validity in the overshadowing of geometric features of an enclosed arena by discrete landmarks were investigated in rats using the water maze paradigm. Experiment 1 established that in a rhomboid-shaped arena, the acute corner was more salient than the obtuse corner. In Experiment 2, rats were trained to find a submerged platform either in one of the acute, or obtuse, corners. In addition to the information provided by corner angle, the platform was also signaled by the presence of a spherical landmark suspended above the platform for rats in the experimental group. The landmark was a more valid cue for predicting the location of the platform than the angle of the corner. This training resulted in overshadowing of learning about the angle of the corner by the presence of the landmark. The final experiment extended this result by showing that when the predictive validities of the angle and the landmark were matched in the experimental group, learning about geometry was still overshadowed by the presence of landmarks, but only in animals that were trained with the platform at an obtuse, but not acute, corner. These results uniquely demonstrate that learning about geometry can be overshadowed by discrete landmarks, and also that whether overshadowing is observed depends on the stimulus salience and the relative validity of the competing cues. These findings imply that learning based on geometric cues follows the same basic rules that apply to a wide range of other learning paradigms.

Spontaneous object recognition memory is maintained following transformation of global geometric properties.

Studies of spontaneous behavior to assess memory are widespread, but often the relationships of objects to contexts and spatial locations are poorly defined. We examined whether object-location memory was maintained following global, but not local, changes to the geometric shape of an arena. Rats explored two trial-unique objects in a distinctively shaped arena before being exposed to two identical copies of one of these objects in a different shape in a different physical location. Rats preferentially explored objects that were novel in relation to their local geometric context rather than identifying both locations as novel in the global geometric context.