The roles of the medial prefrontal cortex and hippocampus in a spatial paired-association task

Although the roles of both the hippocampus and the medial prefrontal cortex (mPFC) have been suggested in a spatial paired-associate memory task, both areas were investigated separately in prior studies. The current study investigated the relative contributions of the hippocampus and mPFC to spatial paired-associate learning within a single behavioral paradigm. In a novel behavioral task, a pair of different objects appeared repeatedly across trials, but in different arms in a radial maze, and different rules were associated with those arms for reward. Specifically, in an "object-in-place" arm, the rat was required to choose a particular object associated with the arm. In a "location-in-place" arm, the animal was required to choose a certain within-arm location (ignoring the object occupying the location). Compared to normal animals, rats with ibotenic acid-based lesions in the hippocampus showed an irrecoverable impairment in performance in both object-in-place and location-in-place arms. When the mPFC was inactivated by muscimol (GABA(A) receptor agonist) in the normal animals with intact hippocampi, they showed the same severe impairment as seen in the hippocampal lesioned rats only in object-in-place arms. The results confirm that the hippocampus is necessary for a biconditional paired-associate task when space is a critical component. The mPFC, however, is more selectively involved in the object-place paired-associate task than in the location-place paired-associate task. The current task powerfully demonstrates an experimental situation in which both the hippocampus and mPFC are required and may serve as a useful paradigm for investigating the neural mechanisms of object-place association.     

Memory for objects and their locations: the role of the hippocampus in retention of object-place associations

Computational models of hippocampal function have suggested that the hippocampus is involved in the formation and storage of arbitrary associations. Previous studies have shown that rats with hippocampal lesions are impaired in object-place associative learning. However, few studies have examined the role of the hippocampus in the retention of previously learned arbitrary associations. In the present study, male Long-Evans rats with either cortical control or hippocampal lesions were tested on a task measuring the retention of previously learned arbitrary associations using an object-place paired-associate task. To assess retention, each animal was trained on the paired-associate task for 360 trials, then received a lesion, and was retested to examine retention of the previously learned associations. The results indicate that all rats learned the task prior to surgery. Following surgery, rats with cortical control lesions were not impaired in the retention of object-place associations. In contrast, hippocampal lesions resulted in an initial deficit in retention of the paired-associate task followed by recovery. Therefore, the hippocampus may play a role in the retrieval of previously learned arbitrary association.     

Has someone moved my plate? The immediate and persistent effects of object location changes on gaze allocation during natural scene viewing

In this study, we investigated the immediate and persisting effects of object location changes on gaze control during scene viewing. Participants repeatedly inspected a randomized set of naturalistic scenes for later questioning. On the seventh presentation, an object was shown at a new location, whereas the change was reversed for all subsequent presentations of the scene. We tested whether deviations from stored scene representations would modify eye movements to the changed regions and whether these effects would persist. We found that changed objects were looked at longer and more often, regardless of change reportability. These effects were most pronounced immediately after the change occurred and quickly leveled off once a scene remained unchanged. However, participants continued to perform short validation checks to changed scene regions, which implies a persistent modulation of eye movement control beyond the occurrence of object location changes.     

The shift from a response strategy to object-in-place strategy during learning is accompanied by a matching shift in neural firing correlates in the hippocampus

Hippocampal-dependent tasks often involve specific associations among stimuli (including egocentric information), and such tasks are therefore prone to interference from irrelevant task strategies before a correct strategy is found. Using an object-place paired-associate task, we investigated changes in neural firing patterns in the hippocampus in association with a shift in strategy during learning. We used an object-place paired-associate task in which a pair of objects was presented in two different arms of a radial maze. Each object was associated with reward only in one of the arms, thus requiring the rats to consider both object identity and its location in the maze. Hippocampal neurons recorded in CA1 displayed a dynamic transition in their firing patterns during the acquisition of the task across days, and this corresponded to a shift in strategy manifested in behavioral data. Specifically, before the rats learned the task, they chose an object that maintained a particular egocentric relationship with their body (response strategy) irrespective of the object identity. However, as the animal acquired the task, it chose an object according to both its identity and the associated location in the maze (object-in-place strategy). We report that CA1 neurons in the hippocampus changed their prospective firing correlates according to the dominant strategy (i.e., response versus object-in-place strategy) employed at a given stage of learning. The results suggest that neural firing pattern in the hippocampus is heavily influenced by the task demand hypothesized by the animal and the firing pattern changes flexibly as the perceived task demand changes.An event often involves objects placed in particular locations. To form a cognitive representation of such an event, an animal needs to represent many heterogeneous pieces of information such as individual objects, their spatial locations, and also egocentric body movements associated with the navigation through the objects and locations. All the information then needs to be associated in a correct way (e.g., proper object-place association) for successful representation of the event. Processing only a subset of information successfully may lead to an error in identifying the correct event. It is believed that the hippocampus is essential for forming and retrieving such conjunctive representations among stimuli for processing events (O''Reilly and McClelland 1994).Due to its conjunctive information processing after receiving inputs from multiple sources (e.g., information for object recognition, egocentric memory, allocentric memory, etc.), the hippocampal system is prone to competition with other systems especially when a simpler strategy that requires information from a single source seems a viable option. Behavioral and pharmacological studies have supported this hypothesis (Packard and McGaugh 1996; Poldrack and Packard 2003). Physiologically, the influence of switching strategy on hippocampal neuronal firing has been documented in the literature and often tested in a plus maze. It has been shown, for example, that passing a common area of space using different task demands alters the firing properties of hippocampal neurons (Wood et al. 2000; Ferbinteanu and Shapiro 2003; Lee et al. 2006; Eschenko and Mizumori 2007). In most of these studies, however, rats were pre-trained before electrophysiological recordings were made and an experimenter enforced the change in task demand. Therefore, it has been difficult to investigate a naturally occurring competition between different strategies as learning proceeds and the resulting neural dynamics in the hippocampus especially when learning takes place for the first time.Using a hippocampal dependent task, we aimed to characterize such naturally occurring changes in hippocampal firing patterns as a wrong strategy is replaced by the correct strategy during learning. We also investigated the relationships between the changes in firing patterns and behavioral performance. We used a biconditional object-place paired-associate task for this purpose. We demonstrated previously that hippocampal lesioned rats were severely impaired in this task (Lee and Solivan 2008). In this task, two different objects are presented simultaneously as a pair, and rats are required to discriminate between the objects according to the location (an arm in a radial maze) in which they are presented. Once it enters an arm, the rat positions itself between two objects and must choose either the left or right direction toward either object to displace the object for obtaining a food reward. Since the relative object positions within an arm vary across trials, remembering the running direction in which a reward is found (i.e., response strategy) is meaningless and the rat must learn to pay attention to the object identity and its associated location in space (i.e., object-in-place strategy). In our previous studies (Lee and Solivan 2008, 2010; Jo and Lee 2010), we observed a strong competition in this task between a response strategy and object-in-place strategy. Normal rats used the response strategy before learning occurred, but exhibited a sharp transition to the object-in-place strategy in several days. The selective involvement of the hippocampus was strongly implicated in the task as the hippocampal lesioned rats show stereotypic egocentric responses (Lee and Solivan 2008). The current study aimed to find and characterize in detail matching neural correlates in the hippocampus in the object-place paired-associate task.     

Imagining what might be: why children underestimate uncertainty

Children’s well-documented tendency to behave as if they know more than they do about uncertain events is reduced under two conditions: when the outcome of a chance event has yet to be determined and when one unknown outcome has occurred but is difficult to imagine. In Experiment 1, in line with published findings, 5- and 6-year-olds (N = 61) preferred to guess the unknown location of a known object when the object was in place rather than before its location had been determined. There was no such preference when the object’s identity was unknown. In Experiment 2, 29 5- and 6-year-olds were more likely to correctly mark both possible locations when an already hidden object’s identity was unknown rather than known. We conclude that children’s vivid imaginations can lead them to underestimate uncertainty in a similar way to imagination inflation or fluency effects in adults.     

A direct assessment of the role of expectation in inhibition of return

An object hidden among distractors can be found more efficiently if previously searched locations are not reinspected. The inhibition-of-return (IOR) phenomenon indexes the tendency to avoid reinspections. Two accounts of IOR, that it is due to inhibition and that it is due to expectation, are generally regarded as incompatible. The relevant evidence to date, however, has been indirect: Inhibition or expectation has been inferred from response times or similar indirect measures. This article reports the first direct measure of IOR, obtained by asking observers to predict the location of the next target in a display containing eight possible locations on an imaginary circle. On any given trial, the previously cued location was chosen less frequently (impairment)--and the opposite location was chosen more frequently (facilitation)--than chance (choice of all other locations was at chance). The impairment is consistent with both inhibition and expectation accounts; the facilitation is consistent only with expectation accounts. This work also shows that inhibition and expectation are not necessarily incompatible: Implementing expectations may entail inhibiting previously cued locations.     

Corticospinal excitability during the observation of social behavior

Evidence suggests that the observation of an action induces in the observers an enhancement of motor evoked potentials (MEPs) recorded by the observer’s muscles corresponding to those involved in the observed action. Although this is a well-studied phenomenon, it remains still unclear how the viewer’s motor facilitation is influenced by the social content characterizing the observed scene. In the present study we investigated the facilitation of the corticospinal system during the observation of either an action that does not imply a social interaction (i.e., an actor throwing a ball against a wall), or an action which implies a social interaction (i.e., an actor passing a ball to a partner). Results indicate that MEPs amplitude is enhanced during the observation of a social rather than an individual action. We contend that the increase in MEPs activation might reflect an enhancement of the simulative activity stemming from the mirror system during the observation of social interactions. Altogether these findings show that the human corticospinal system is sensitive to social interactions and may support the role of the mirror neurons system in social cognition.     

Decoding facial blends of emotion: Visual field,attentional and hemispheric biases

Most clinical research assumes that modulation of facial expressions is lateralized predominantly across the right-left hemiface. However, social psychological research suggests that facial expressions are organized predominantly across the upper-lower face. Because humans learn to cognitively control facial expression for social purposes, the lower face may display a false emotion, typically a smile, to enable approach behavior. In contrast, the upper face may leak a person’s true feeling state by producing a brief facial blend of emotion, i.e. a different emotion on the upper versus lower face. Previous studies from our laboratory have shown that upper facial emotions are processed preferentially by the right hemisphere under conditions of directed attention if facial blends of emotion are presented tachistoscopically to the mid left and right visual fields. This paper explores how facial blends are processed within the four visual quadrants. The results, combined with our previous research, demonstrate that lower more so than upper facial emotions are perceived best when presented to the viewer’s left and right visual fields just above the horizontal axis. Upper facial emotions are perceived best when presented to the viewer’s left visual field just above the horizontal axis under conditions of directed attention. Thus, by gazing at a person’s left ear, which also avoids the social stigma of eye-to-eye contact, one’s ability to decode facial expressions should be enhanced.     

Hippocampus is required for paired associate memory with neither delay nor trial uniqueness

Cued retrieval of memory is typically examined with delay when testing hippocampal functions, as in delayed matching-to-sample tasks. Equally emphasized in the literature, on the other hand, is the hippocampal involvement in making arbitrary associations. Paired associate memory tasks are widely used for examining this function. However, the two variables (i.e., delay and paired association) were often mixed in paired associate tasks, and this makes it difficult to localize the cognitive source of deficits with hippocampal perturbation. Specifically, a few studies have recently shown that rats can learn arbitrary paired associations between certain locations and nonspatial items (e.g., object or flavor) and later can retrieve the paired location when cued by the item remotely. Such tasks involve both (1) delay between sampling the cue and retrieving the target location and (2) arbitrary association between the cueing object and its paired location. Here, we tested whether delay was necessary in a cued paired associate task by using a task in which no delay existed between object cueing and the choice of its paired associate. Moreover, fixed associative relationships between the cueing objects and their paired locations were repeatedly used, thus involving no trial-unique association. Nevertheless, inactivations of the dorsal hippocampus with muscimol severely disrupted retrieval of paired associates, whereas the same manipulations did not affect discriminating individual objects or locations. The results powerfully demonstrate that the hippocampus is inherently required for retrieving paired associations between objects and places, and that delay and trial uniqueness of the paired associates are not necessarily required.     

The posterior parietal cortex and long-term memory representation of spatial information

The hypothesis to be explored in this chapter is based on the assumption that the posterior parietal cortex (PPC) is directly involved in representing a subset of the spatial features associated with spatial information processing and plays an important role in perceptual memory as well as long-term memory encoding, consolidation, and retrieval of spatial information. After presentation of the anatomical location of the PPC in rats, the nature of PPC representation based on single spatial features, binding of visual features associated with visual spatial attention, binding of object-place associations associated with acquisition and storage of associations where one of the elements is a spatial component, and binding of ideothetic and allothetic information in long-term memory is discussed. Additional evidence for a PPC role in mediation of spatial information in long-term storage is offered. Finally, the relationship between the PPC and the hippocampus from a systems and dynamic point view is presented.     

Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats

The positive impact of sleep on memory consolidation has been shown for human subjects in numerous studies, but there is still sparse knowledge on this topic in rats, one of the most prominent model species in neuroscience research. Here, we examined the role of sleep in the object-place recognition task, a task closely comparable to tasks typically applied for testing human declarative memory: It is a one-trial task, hippocampus-dependent, not stressful and can be repeated within the same animal. A test session consisted of the Sample trial, followed by a 2-h retention interval and a Test trial, the latter examining the memory the rat had for the places of two objects presented at the Sample trial. In Experiment 1, each rat was tested twice, with the retention interval taking place either in the morning or evening, i.e., in the inactive or active phase, respectively. Rats showed significantly (p<0.01) better memory for object place after the Morning session. To control for confounding circadian factors, in Experiment 2 rats were tested four times, i.e., in the morning or in the evening while sleep was or was not deprived. Sleep during the retention interval was recorded polysomnographically. Rats only showed significant memory for the target object place in the Test trial after the Morning retention interval in the absence of sleep deprivation, and recognition performance in this condition was significantly superior to that in the three other conditions (p<0.05). EEG recordings during spontaneous morning sleep revealed increased slow oscillation (0.85-2.0 Hz) and upper delta (2.0-4.0 Hz), but reduced spindle band (10.5-13.5 Hz) activity, as compared to evening sleep. However, spindle band power was increased in the Morning retention interval in comparison to a Morning Baseline period (p<0.05). We conclude that consolidation of object-place memory depends on sleep, and presumably requires NonREM sleep rich in both slow wave and spindle activity.     

Spatial updating of dynamic scenes: Tracking multiple invisible objects across viewpoint changes

Research on dynamic attention has shown that visual tracking is possible even if the observer’s viewpoint on the scene holding the moving objects changes. In contrast to smooth viewpoint changes, abrupt changes typically impair tracking performance. The lack of continuous information about scene motion, resulting from abrupt changes, seems to be the critical variable. However, hard onsets of objects after abrupt scene motion could explain the impairment as well. We report three experiments employing object invisibility during smooth and abrupt viewpoint changes to examine the influence of scene information on visual tracking, while equalizing hard onsets of moving objects after the viewpoint change. Smooth viewpoint changes provided continuous information about scene motion, which supported the tracking of temporarily invisible objects. However, abrupt and, therefore, discontinuous viewpoint changes strongly impaired tracking performance. Object locations retained with respect to a reference frame can account for the attentional tracking that follows invisible objects through continuous scene motion.     

Prolonged inactivation of the hippocampus reveals temporally graded retrograde amnesia for unreinforced spatial learning in rats

We investigated whether systems consolidation of spatial memory could be detected in a non-navigational, spatial-learning test that takes advantage of rats’ natural propensity to preferentially investigate an object that was displaced relative to spatial cues more than an object that remained stationary. Previous studies using navigational spatial-learning tests have generally failed to reveal temporally-graded retrograde amnesia, possibly because the hippocampus needs to be intact for the retrieval and/or processing of navigational information during the test. In the present study, the hippocampus of rats was kept inactivated, at two sites along its septo-temporal axis (dorsal and intermediate), for four consecutive days, beginning either 3 h or 5 days after familiarization to two identical objects in an open field. Rats that had their hippocampus inactivated beginning 5 days but not 3 h after familiarization showed evidence that they remembered the previous location of the displaced object. The results suggest that systems consolidation of spatial memories can be detected using a non-navigational test of spatial memory.     

The effect of spatial and nonspatial contextual information on visual object memory

Recent research has found visual object memory can be stored as part of a larger scene representation rather than independently of scene context. The present study examined how spatial and nonspatial contextual information modulate visual object memory. Two experiments tested participants’ visual memory by using a change detection task in which a target object's orientation was either the same as it appeared during initial viewing or changed. In addition, we examined the effect of spatial and nonspatial contextual manipulations on change detection performance. The results revealed that visual object representations can be maintained reliably after viewing arrays of objects. Moreover, change detection performance was significantly higher when either spatial or nonspatial contextual information remained the same in the test image. We concluded that while processing complex visual stimuli such as object arrays, visual object memory can be stored as part of a comprehensive scene representation, and both spatial and nonspatial contextual changes modulate visual memory retrieval and comparison.     

Implicit scene learning is viewpoint dependent

When novel scenes are encoded, the representations of scene layout are generally viewpoint specific. Past studies of scene recognition have typically required subjects to explicitly study and encode novel scenes, but in everyday visual experience, it is possible that much scene learning occurs incidentally. Here, we examine whether implicitly encoded scene layouts are also viewpoint dependent. We used the contextual cuing paradigm, in which search for a target is facilitated by implicitly learned associations between target locations and novel spatial contexts (Chun & Jiang, 1998). This task was extended to naturalistic search arrays with apparent depth. To test viewpoint dependence, the viewpoint of the scenes was varied from training to testing. Contextual cuing and, hence, scene context learning decreased as the angular rotation from training viewpoint increased. This finding suggests that implicitly acquired representations of scene layout are viewpoint dependent.     

Do people automatically track others’ beliefs? Evidence from a continuous measure

Recent findings suggest that tracking others’ beliefs is not always effortful and slow, but may rely on a fast and implicit system. An untested prediction of the automatic belief tracking account is that own and others’ beliefs should be activated in parallel. We tested this prediction measuring continuous movement trajectories in a task that required deciding between two possible object locations. We independently manipulated whether participants’ belief about the object location was true or false and whether an onlooker’s belief about the object location was true or false. Manipulating whether or not the agent’s belief was ever task relevant allowed us to compare performance in an explicit and implicit version of the same task. Movement parameters revealed an influence of the onlooker’s irrelevant belief in the implicit version of the task. This provides evidence for parallel activation of own and others’ beliefs.     

“Mother nature doesn’t have a bullet with your name on it”: Coding with reference to one’s name or object location?

When movements of a joystick toward/away from the self are made in response to positive/negative words, performance is better with the positive-toward/negative-away mapping than with the alternative mapping, consistent with an approach-avoidance motivational account. Markman and Brendl (2005) instructed participants to move a positive or negative word toward or away from their name, located on a bar at the center of a three-dimensional display. The positive-toward/negative-away mapping relative to the name’s location was preferred, which means that relative to the body the preferred mapping reversed to positive-away/negative-toward when the word was in front of the name. This finding was interpreted as demonstrating that “the compatibility effect depends on people’s representation of their selves in space rather than on their physical location” (p. 6). Alternatively, this effect may arise from the bar providing a salient referent object for coding relative location. We report an experiment that replicates these findings but shows similar results when there is no name on the bar and/or no three-dimensional perspective. An account in terms of action effects involving implied movement of the word toward or away from a referent object rather than a representation of self provides the simplest explanation of the compatibility effect.     

Conceptual knowledge attenuates viewpoint dependency in visual object recognition

Learning verbal semantic knowledge for objects has been shown to attenuate recognition costs incurred by changes in view from a learned viewpoint. Such findings were attributed to the semantic or meaningful nature of the learned verbal associations. However, recent findings demonstrate surprising benefits to visual perception after learning even noninformative verbal labels for stimuli. Here we test whether learning verbal information for novel objects, independent of its semantic nature, can facilitate a reduction in viewpoint-dependent recognition. To dissociate more general effects of verbal associations from those stemming from the semantic nature of the associations, participants learned to associate semantically meaningful (adjectives) or nonmeaningful (number codes) verbal information with novel objects. Consistent with a role of semantic representations in attenuating the viewpoint-dependent nature of object recognition, the costs incurred by a change in viewpoint were attenuated for stimuli with learned semantic associations relative to those associated with nonmeaningful verbal information. This finding is discussed in terms of its implications for understanding basic mechanisms of object perception as well as the classic viewpoint-dependent nature of object recognition.     

Adoption of an internal viewpoint following presentations of plan‐view diagrams and maps

This study investigated people's ability to adopt novel imagined viewpoints after studying plan‐view diagrams and maps. In two experiments, university students were presented with a plan‐view diagram of a character surrounded by nearby objects (Expt 1) or a character within a map of a multi‐level shopping centre (Expt 2). Subsequently, participants' spatial knowledge of the diagrams/maps was tested by asking them about the location of six salient objects/places. In both experiments, the analyses of participants' spatial judgments suggested that they had adopted an imagined viewpoint internal to the character. The findings add to our understanding of imagined viewpoint switches along the vertical axis of space.     

Mapping visual attention with change blindness: new directions for a new method

Change blindness provides a new technique for mapping visual attention with unprecedented spatial and temporal resolution. Change blindness can occur when a brief full-field blank interferes with the detection of changes in a scene that occur during the blank. This interference can be overcome by attending to the location of a change. Because changes are detected at attended locations, but not at unattended locations, detection accuracy provides an indirect measure of the distribution of visual attention. The likelihood of detecting a new element in a scene provides a measure of the occurrence of attention at that element’s location. Potential new directions, advantages, and problems with this method are considered.