A model of episodic memory: Mental time travel along encoded trajectories using grid cells

The definition of episodic memory includes the concept of mental time travel: the ability to re-experience a previously experienced trajectory through continuous dimensions of space and time, and to recall specific events or stimuli along this trajectory. Lesions of the hippocampus and entorhinal cortex impair human episodic memory function and impair rat performance in tasks that could be solved by retrieval of trajectories. Recent physiological data suggests a novel model for encoding and retrieval of trajectories, and for associating specific stimuli with specific positions along the trajectory. During encoding in the model, external input drives the activity of head direction cells. Entorhinal grid cells integrate the head direction input to update an internal representation of location, and drive hippocampal place cells. Trajectories are encoded by Hebbian modification of excitatory synaptic connections between hippocampal place cells and head direction cells driven by external action. Associations are also formed between hippocampal cells and sensory stimuli. During retrieval, a sensory input cue activates hippocampal cells that drive head direction activity via previously modified synapses. Persistent spiking of head direction cells maintains the direction and speed of the action, updating the activity of entorhinal grid cells that thereby further update place cell activity. Additional cells, termed arc length cells, provide coding of trajectory segments based on the one-dimensional arc length from the context of prior actions or states, overcoming ambiguity where the overlap of trajectory segments causes multiple head directions to be associated with one place. These mechanisms allow retrieval of complex, self-crossing trajectories as continuous curves through space and time.     

Flexible cue use in food-caching birds

An animal’s memory may be limited in capacity, which may result in competition among available memory cues. If such competition exists, natural selection may favor prioritization of different memory cues based on cue reliability and on associated differences in the environment and life history. Food-caching birds store numerous food items and appear to rely on memory to retrieve caches. Previous studies suggested that caching species should always prioritize spatial cues over non-spatial cues when both are available, because non-spatial cues may be unreliable in a changing environment; however, it remains unclear whether non-spatial cues should always be ignored when spatial cues are available. We tested whether mountain chickadees (Poecile gambeli), a food-caching species, prioritize memory for spatial cues over color cues when relocating previously found food in an associative learning task. In training trials, birds were exposed to food in a feeder where both spatial location and color were associated. During subsequent unrewarded test trials, color was dissociated from spatial location. Chickadees showed a significant pattern of inspecting feeders associated with correct color first, prior to visiting correct spatial locations. Our findings argue against the hypothesis that the memory of spatial cues should always take priority over any non-spatial cues, including color cues, in food-caching species, because in our experiment mountain chickadees chose color over spatial cues. Our results thus suggest that caching species may be more flexible in cue use than previously thought, possibly dependent upon the environment and complexity of available cues.     

Comparing black-capped (Poecile atricapillus) and mountain chickadees (Poecile gambeli): use of geometric and featural information in a spatial orientation task

Since Cheng (Cognition 23:149–178, 1986) first proposed the “geometric module” in rats, a great deal of research has focused on how other species use geometric information and how geometric encoding may differ across species. Here, hand-reared and wild-caught black-capped chickadees and wild-caught mountain chickadees searched for food hidden in one corner in a rectangular environment. Previous research has shown that mountain chickadees do not spontaneously encode geometric information when a salient feature is present near the goal location. Using a slightly different training and testing procedure, we found that both hand-reared and wild-caught black-capped chickadees encoded geometric information, even in the presence of a salient landmark. Some, but not all, mountain chickadees also encoded geometric information. Overall, our results suggest that use of geometric information may be a less preferred strategy for mountain chickadees than for either wild-caught or hand-reared black-capped chickadees. To our knowledge, this is the first direct interspecies comparison of use of geometric information in a spatial orientation task.     

Spatial cognition in the gerbil: computing optimal escape routes from visual threats

Previous studies in our laboratory have shown that when presented with a sudden stimulus simulating an oncoming predator, Mongolian gerbils can compute the optimal trajectory to a safe refuge, taking into account the position of the threat, the location of a clearly visible refuge, and several other contextual variables as well. In the present studies, the main goal was to explore the abilities of gerbils to use mental representations of spaces that were visually occluded by opaque barriers to compute efficient escape trajectories. In all studies, gerbils were placed into a round open field containing a single refuge. On each trial, an overhead visual stimulus was caused to ‘fly’ overhead, eliciting robust escape movements from the gerbils. By manipulating the shape and position of a series of opaque barriers that were interposed between the gerbils and the refuge, we were able to show that gerbils can compute the shortest route to an invisible target, even when the available routes to the target are made complex by using elaborate barrier shapes. These findings suggest that gerbils can maintain representations of their locations with respect to salient environmental landmarks and refuges, even when such locations are not continuously visible.     

Flexible use of spatial cues in the southern flying squirrel (<Emphasis Type="Italic">Glaucomys volans</Emphasis>)

Insects, birds, and mammals have been shown capable of encoding spatial information in memory using multiple strategies or frames of reference simultaneously. These strategies include orientation to a goal-specific cue or beacon, to the position of the goal in an array of local landmarks, or to its position in the array of distant landmarks, also known as the global frame of reference. From previous experiments, it appears that birds and mammals that scatter hoard rely primarily on a global frame of reference, but this generalization depends on evidence from only a few species. Here we examined spatial memory in a previously unstudied scatter hoarder, the southern flying squirrel. We dissociated the relative weighting of three potential spatial strategies (beacon, global, or relative array strategy) with three probe tests: transposition of beacon and the rotation or the expansion of the array. The squirrels’ choices were consistent with a spatial averaging strategy, where they chose the location dictated by at least two of the three strategies, rather than using a single preferred frame of reference. This adaptive and flexible heuristic has not been previously described in animal orientation studies, yet it may be a common solution to the universal problem of encoding and recalling spatial locations in an ephemeral physical landscape.     

Spider monkey ranging patterns in Mexican subtropical forest: do travel routes reflect planning?

Although it is well known that frugivorous spider monkeys (Ateles geoffroyi yucatanensis) occupy large home ranges, travelling long distances to reach highly productive resources, little is known of how they move between feeding sites. A 11 month study of spider monkey ranging patterns was carried out at the Otochma’ax Yetel Kooh reserve, Yucatán, Mexico. We followed single individuals for as long as possible each day and recorded the routes travelled with the help of a GPS (Global Positioning System) device; the 11 independently moving individuals of a group were targeted as focal subjects. Travel paths were composed of highly linear segments, each typically ending at a place where some resource was exploited. Linearity of segments did not differ between individuals, and most of the highly linear paths that led to food resources were much longer than the estimate visibility in the woodland canopy. Monkeys do not generally continue in the same ranging direction after exploiting a resource: travel paths are likely to deviate at the site of resource exploitation rather than between such sites. However, during the harshest months of the year consecutive route segments were more likely to retain the same direction of overall movement. Together, these findings suggest that while moving between feeding sites, spider monkeys use spatial memory to guide travel, and even plan more than one resource site in advance. This contribution is part of the special issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

The impact of landmark properties in shaping exploration and navigation

This study was aimed at uncovering physical and geometric properties that make a particular landmark a target of exploration and navigation. Rats were tested in a square open-field arena with additional portable corners featuring the same properties as the arena corners. It was found that the routes of progression converged upon the added corners, whether located at the arena wall or the arena center. Route convergence upon the added corners involved numerous visits to these corners. However, time spent at the added corners was relatively short compared with the arena corners, including that from which rats were introduced into the arena. There was no differential effect of testing rats in light or dark, or with a low versus a high portable corner. It is suggested that the added corners were distinct against the background of the arena enclosure, whereas the four arena corners and walls were encoded by the rats as one geometric module. This distinctness, together with the greater accessibility of the added corners, made them salient landmarks and a target of exploration. Thus, the impact of a landmark extended beyond its specific self-geometry to include accessibility and distinctness, which are contextual properties. In addition to the contextual impact on locomotor behavior there was also a temporal effect, with security initially dominating the rats’ behavior but then declining along with an increased attraction to salient landmarks. These spatiotemporal patterns characterized behavior in both lit and dark arenas, indicating that distal cues were secondary to local proximal cues in shaping routes.     

Skill theory v2.0: dispositions,emulation, and spatial perception

An attempt is made to defend a general approach to the spatial content of perception, an approach according to which perception is imbued with spatial content in virtue of certain kinds of connections between perceiving organism’s sensory input and its behavioral output. The most important aspect of the defense involves clearly distinguishing two kinds of perceptuo-behavioral skills—the formation of dispositions, and a capacity for emulation. The former, the formation of dispositions, is argued to by the central pivot of spatial content. I provide a neural information processing interpretation of what these dispositions amount to, and describe how dispositions, so understood, are an obvious implementation of Gareth Evans’ proposal on the topic. Furthermore, I describe what sorts of contribution are made by emulation mechanisms, and I also describe exactly how the emulation framework differs from similar but distinct notions with which it is often unhelpfully confused, such as sensorimotor contingencies and forward models.     

Hand function,not proximity,biases visuotactile integration later in object processing: An ERP study

Behavioral studies document a functional hand proximity effect: objects near the palm, but not the back of the hand, affect visual processing. Although visuotactile bimodal neurons integrate visual and haptic inputs, their receptive fields in monkey cortex encompass the whole hand, not just the palm. Using ERPs, we investigated whether hand function influenced the topology of integrated space around the hand. In a visual detection paradigm, target and non-target stimuli appeared equidistantly in front or in back of the hand. Equivalent N1 amplitudes were found for both conditions. P3 target versus non-target amplitude differences were greater for palm conditions. Hand proximity biased processing of visual targets equidistant from the hand early in processing. However, hand function biases emerged later when targets were selected for potential action. Thus, early hand proximity effects on object processing depend on sensory-reliant neural responses, whereas later multisensory integration depend more on the hand’s functional expertise.