Spatial Cognition in Teleost Fish: Strategies and Mechanisms

Teleost fish have been traditionally considered primitive vertebrates compared to mammals and birds in regard to brain complexity and behavioral functions. However, an increasing amount of evidence suggests that teleosts show advanced cognitive capabilities including spatial navigation skills that parallel those of land vertebrates. Teleost fish rely on a multiplicity of sensory cues and can use a variety of spatial strategies for navigation, ranging from relatively simple body-centered orientation responses to allocentric or “external world-centered” navigation, likely based on map-like relational memory representations of the environment. These distinct spatial strategies are based on separate brain mechanisms. For example, a crucial brain center for egocentric orientation in teleost fish is the optic tectum, which can be considered an essential hub in a wider brain network responsible for the generation of egocentrically referenced actions in space. In contrast, other brain centers, such as the dorsolateral telencephalic pallium of teleost fish, considered homologue to the hippocampal pallium of land vertebrates, seem to be crucial for allocentric navigation based on map-like spatial memory. Such hypothetical relational memory representations endow fish’s spatial behavior with considerable navigational flexibility, allowing them, for example, to perform shortcuts and detours.

Threat impairs flexible use of a cognitive map

Goal-directed behavior requires adaptive systems that respond to environmental demands. In the absence of threat (or presence of reward), individuals are free to explore a large number of behavioral trajectories, effectively interrogating the environment across many dimensions. This leads to flexible, relational memory encoding and retrieval. In the presence of imminent danger, motivation shifts to an imperative state characterized by a narrow focus of attention on threatening information. This impairs flexible, relational memory. Here, we test how these proposed motivational shifts (Murty & Adcock, 2017) affect behavioral flexibility and memory. Participants learned the structure of a maze-like environment and navigated to the location of everyday objects in both safe and threatening contexts. The latter contained a predator that could ‘capture’ participants, leading to electric shock. After learning, the path to some objects was blocked, forcing a detour for which one route was significantly shorter. We predicted that the threatening environment would push participants toward an imperative state, leading to less efficient and less flexible navigation. Across 3 studies, we found that threat caused participants to take longer paths to goal objects and less efficient detours when obstacles were encountered. Navigation was less efficient despite no impairment in recognition memory for the maps learned in safe vs threatening contexts. These results provide ecologically valid evidence that imperative states, triggered by threat, reduce the ability to flexibly use cognitive maps to guide behavior.

The Role of the Ventromedial Prefrontal Cortex and Basal Forebrain in Relational Memory and Inference

The ventromedial prefrontal cortex (vMPFC) is involved in diverse cognitive operations, from inhibitory control to processing of semantic schemas. When accompanied by damage to the basal forebrain, vMPFC lesions can also impair relational memory, the ability to form and recall relations among items. Impairments in establishing direct relations among items (e.g., A is related to B, B is related to C) can also hinder the transitive processing of indirect relationships (e.g., inferring that A and C are related through direct relations that each contain B). Past work has found that transitive inference improves when the direct relations are organized within an existing knowledge structure, or schema. This type of semantic support is most effective for individuals whose relational memory deficits are mild (e.g., healthy age-related decline) rather than pronounced (e.g., hippocampal amnesia, amnestic mild cognitive impairment). Given that vMPFC damage can produce both relational memory and schema processing deficits, such damage may pose a particular challenge in establishing the type of relational structure required for transitive inference, even when supported by preexisting knowledge. To examine this idea, we tested individuals with lesions to the MPFC on multiple conditions that varied in pre-experimental semantic support and explored the extent to which they could identify both previously studied (direct) and novel transitive (indirect) relations. Most of the MPFC cases showed marked transitive inference deficits and even showed impaired knowledge of preexisting, direct, semantic relations, consistent with disruptions to schema-related processes. However, one case with more dorsal MPFC damage showed preserved ability to identify direct relations and make novel inferences, particularly when pre-experimental knowledge could be used to support performance. These results suggest that damage to the MPFC and basal forebrain can impede establishment of ad hoc relational schemas upon which transitive inference is based, but that appealing to prior knowledge may still be useful for those neurological cases that have some degree of preserved relational memory.

Threat learning impairs subsequent memory recombination with past episodes

To successfully predict important events, the representations in memory on which we rely need to be constantly updated and transformed to best reflect a complex and dynamic world. Here we employed a novel paradigm to investigate how memories of threat learning affect the flexible recombination across distinct but overlapping experiences, an ability referred to as relational memory. Participants (n=35) visited the lab to first encode neutral associations (A - B), which were reactivated and predictively associated with a new aversive or neutral element (B - C) on the following day, whilst pupil dilation was measured as an index of arousal. Then, again one day later, the accuracy of relational memory judgements (A - C?) was tested. Novel association to threat was found to impair relational memory. Unexpectedly, this effect was not moderated by arousal. We propose that compartmentalization of threat learning events could be a function of a healthy memory, preventing maladaptive ‘episodic overgeneralization’ of threat to previously encoded episodes.

Intrinsic hippocampal functional connectivity underlying rigid memory in children and adolescents with autism spectrum disorder: A case–control study

Atypical learning and memory in early life can promote atypical behaviors in later life. Less relational learning and inflexible retrieval in childhood may enhance restricted and repeated behaviors in patients with autism spectrum disorder. The purpose of this study was to elucidate the mechanisms of atypical memory in children with autism spectrum disorder. We conducted picture–name pair learning and delayed-recognition tests with two groups: one group with high-functioning autism spectrum disorder children (aged 7–16, n = 41) and one group with typically developing children ( n = 82) that matched the first group’s age, sex, and IQ. We assessed correlations between successful recognition scores and seed-to-whole-brain resting-state functional connectivity. Although both learning and retrieval performances were comparable between the two groups, we observed slightly lower category learning and significantly fewer memory gains in the autism spectrum disorder group than in the typically developing group. The right canonical anterior hippocampal network was involved in successful memory in youths with typically developing, while other memory systems may be involved in successful memory in youths with autism spectrum disorder. Context-independent and less relational memory processing may be associated with fewer memory gains in autism spectrum disorder. These atypical memory characteristics in autism spectrum disorder may accentuate their inflexible behaviors in some situations. Lay abstract Atypical learning and memory in early life can promote atypical behaviors in later life. Specifically, less relational learning and inflexible retrieval in childhood may enhance restricted and repeated behaviors in patients with autism spectrum disorder. The purpose of this study was to elucidate the mechanisms of atypical memory in children with autism spectrum disorder. We conducted picture–name pair learning and delayed-recognition tests with two groups of youths: one group with high-functioning autism spectrum disorder children (aged 7–16, n = 41) and one group with typically developing children ( n = 82) that matched the first group’s age, sex, and full-scale IQ. We examined correlations between successful recognition scores and neural connectivity during resting in the magnetic resonance imaging scanner without thinking about anything. Although both learning and retrieval performances were comparable between the two groups, we observed significantly fewer memory gains in the autism spectrum disorder group than in the typically developing group. The memory network was involved in successful memory retrieval in youths with typically developing, while the other memory systems that do not depend to a great degree on networks may be involved in successful memory in youths with autism spectrum disorder. Context-independent and less relational memory processing may be associated with fewer memory gains in autism spectrum disorder. In other words, autism spectrum disorder youths might benefit from non-relational memory. These atypical memory characteristics in autism spectrum disorder may exaggerate their inflexible behaviors in some situations, or—vice versa—their atypical behaviors may result in rigid and less connected memories.

Aerobic Fitness Unrelated to Acquisition of Spatial Relational Memory in College-Aged Adults

While compelling evidence indicates that poorer aerobic fitness relates to impairments in retrieving information from hippocampal-dependent memory, there is a paucity of research on how aerobic fitness relates to the acquisition of such relational information. Accordingly, the present investigation examined the association between aerobic fitness and the rate of encoding spatial relational memory—assessed using a maximal oxygen consumption test and a spatial configuration task—in a sample of 152 college-aged adults. The findings from this investigation revealed no association between aerobic fitness and the acquisition of spatial relational memory. These findings have implications for how aerobic fitness is characterized with regard to memory, such that aerobic fitness does not appear to relate to the rate of learning spatial–relational information; however, given previously reported evidence, aerobic fitness may be associated with a greater ability to recall relational information from memory.