The Versatile Wayfinder: Prefrontal Contributions to Spatial Navigation

Highlights: Navigation is a behavior fundamental to all mobile animals, and incorporates various cognitive functions, including memory, planning, decision-making, and updating models of the world. Historically, the neural underpinnings of flexible navigation have focused on the hippocampal formation, but recent evidence suggests that regions of the prefrontal cortex (PFC) are crucial to many aspects of navigation, especially when environments are complex or dynamic. This review summarizes what we know from recent human, non-human primate, and rodent studies, proposing a novel perspective that incorporates our knowledge across species and brain regions seeking to avoid tunnel vision in understanding the multifaceted behavior in navigation

Human Navigation: Occipital Place Area Detects Potential Paths in a Scene

Navigation — determining how to get from where you are to somewhere else — has obvious importance for the survival of motile animals. A new neuroimaging study has revealed that, in the human brain, the occipital place area detects the number of possible paths in a vista

Emotional distraction in the context of memory-based orienting of attention

Attention can be guided by expectations stemming from long-term memories. In addition to such endogenous cues, exogenous salient stimuli capture attention, such as those conveying threat. This study examined the extent to which threatening distractors affect the employment of memories in guiding attention, and whether this is affected by trait anxiety. Emotional distractors were incorporated into a speeded target detection task, in which memory cues were presented simultaneously with task irrelevant emotional faces. Fearful face distractors disrupted target detection significantly more than neutral faces and the additional disruption to task performance from fearful compared with neutral faces was positively correlated with trait anxiety scores. The current findings of attentional capture by threat in the context of a second, powerful endogenous driver of attention underscore the magnitude of anxiety-related attention to threat. That is, threatening stimuli are sufficiently salient to induce prolonged disruption to goal directed behavior in anxious individuals. (PsycINFO Database Record (c) 2019 APA, all rights reserved)

Cognitive mapping style relates to posterior-anterior hippocampal volume ratio

As London taxi drivers acquire "the knowledge" and develop a detailed cognitive map of London, their posterior hippocampi (pHPC) gradually increase in volume, reflecting an increasing pHPC/aHPC volume ratio. In the mnemonic domain, greater pHPC/aHPC volume ratios in young adults have been found to relate to better recollection ability, indicating that the balance between pHPC and aHPC volumes might be reflective of cross-domain individual differences. Here, we examined participants' self-reported use of cognitive map-based navigational strategies in relation to their pHPC/aHPC hippocampal volume ratio. We find that greater reported cognitive map use was related to significantly greater posterior, relative to anterior, hippocampal volume in two separate samples of young adults. Further, greater reported cognitive map usage correlated with better performance on a self-initiated navigation task. Together, these data help to advance our understanding of differences between aHPC and pHPC and the greater role of pHPC in spatial mapping

Is attention based on spatial contextual memory preferentially guided by low spatial frequency signals?

A popular model of visual perception states that coarse information (carried by low spatial frequencies) along the dorsal stream is rapidly transmitted to prefrontal and medial temporal areas, activating contextual information from memory, which can in turn constrain detailed input carried by high spatial frequencies arriving at a slower rate along the ventral visual stream, thus facilitating the processing of ambiguous visual stimuli. We were interested in testing whether this model contributes to memory-guided orienting of attention. In particular, we asked whether global, low-spatial frequency (LSF) inputs play a dominant role in triggering contextual memories in order to facilitate the processing of the upcoming target stimulus. We explored this question over four experiments. The first experiment replicated the LSF advantage reported in perceptual discrimination tasks by showing that participants were faster and more accurate at matching a low spatial frequency version of a scene, compared to a high spatial frequency version, to its original counterpart in a forced-choice task. The subsequent three experiments tested the relative contributions of low versus high spatial frequencies during memory-guided covert spatial attention orienting tasks. Replicating the effects of memory-guided attention, pre-exposure to scenes associated with specific spatial memories for target locations (memory cues) led to higher perceptual discrimination and faster response times to identify targets embedded in the scenes. However, either high or low spatial frequency cues were equally effective; LSF signals did not selectively or preferentially contribute to the memory-driven attention benefits to performance. Our results challenge a generalized model that LSFs activate contextual memories, which in turn bias attention and facilitate perception

Preserved memory-based orienting of attention with impaired explicit memory in healthy ageing.

It is increasingly recognised that spatial contextual long-term memory (LTM) prepares neural activity for guiding visuo-spatial attention in a proactive manner. In the current study, we investigated whether the decline in explicit memory observed in healthy ageing would compromise this mechanism. We compared the behavioural performance of younger and older participants on learning new contextual memories, on orienting visual attention based on these learnt contextual associations, and on explicit recall of contextual memories. We found a striking dissociation between older versus younger participants in the relationship between the ability to retrieve contextual memories versus the ability to use these to guide attention to enhance performance on a target-detection task. Older participants showed significant deficits in the explicit retrieval task, but their behavioural benefits from memory-based orienting of attention were equivalent to those in young participants. Furthermore, memory-based orienting correlated significantly with explicit contextual LTM in younger adults but not in older adults. These results suggest that explicit memory deficits in ageing might not compromise initial perception and encoding of events. Importantly, the results also shed light on the mechanisms of memory-guided attention, suggesting that explicit contextual memories are not necessary

Reward associations magnify memory-based biases on perception.

Long-term spatial contextual memories are a rich source of predictions about the likely locations of relevant objects in the environment and should enable tuning of neural processing of unfolding events to optimize perception and action. Of particular importance is whether and how the reward outcome of past events can impact perception. We combined behavioral measures with recordings of brain activity with high temporal resolution to test whether the previous reward outcome associated with a memory could modulate the impact of memory-based biases on perception, and if so, the level(s) at which visual neural processing is biased by reward-associated memory-guided attention. Data showed that past rewards potentiate the effects of spatial memories upon the discrimination of target objects embedded within complex scenes starting from early perceptual stages. We show that a single reward outcome of learning impacts on how we perceive events in our complex environments

Preserved memory-based orienting of attention with impaired explicit memory in healthy ageing.

It is increasingly recognised that spatial contextual long-term memory (LTM) prepares neural activity for guiding visuo-spatial attention in a proactive manner. In the current study, we investigated whether the decline in explicit memory observed in healthy ageing would compromise this mechanism. We compared the behavioural performance of younger and older participants on learning new contextual memories, on orienting visual attention based on these learnt contextual associations, and on explicit recall of contextual memories. We found a striking dissociation between older versus younger participants in the relationship between the ability to retrieve contextual memories versus the ability to use these to guide attention to enhance performance on a target-detection task. Older participants showed significant deficits in the explicit retrieval task, but their behavioural benefits from memory-based orienting of attention were equivalent to those in young participants. Furthermore, memory-based orienting correlated significantly with explicit contextual LTM in younger adults but not in older adults. These results suggest that explicit memory deficits in ageing might not compromise initial perception and encoding of events. Importantly, the results also shed light on the mechanisms of memory-guided attention, suggesting that explicit contextual memories are not necessary

Apolipoprotein ε4 breaks the association between declarative long-term memory and memory-based orienting of spatial attention in middle-aged individuals

Apolipoprotein (APOE) ε4 genotype has been identified as a risk factor for late-onset Alzheimer disease (AD). The memory system is mostly involved in AD, and memory deficits represent its key feature. A growing body of studies has focused on the earlier identification of cognitive dysfunctions in younger and older APOE ε4 carriers, but investigation on middle-aged individuals remains rare. Here we sought to investigate if the APOE ε4 genotype modulates declarative memory and its influences on perception in the middle of the life span. We tested 60 middle-aged individuals recruited according to their APOE allele variants (ε3/ε3, ε3/ε4, ε4/ε4) on a long-term memory-based orienting of attention task. Results showed that the APOE ε4 genotype impaired neither explicit memory nor memory-based orienting of spatial attention. Interestingly, however, we found that the possession of the ε4 allele broke the relationship between declarative long-term memory and memory-guided orienting of visuo-spatial attention, suggesting an earlier modulation exerted by pure genetic characteristics on cognition. These findings are discussed in light of possible accelerated brain ageing in middle-aged ε4-carriers, and earlier structural changes in the brain occurring at this stage of the lifespan

The functional consequences of social distraction: Attention and memory for complex scenes

Cognitive scientists have long proposed that social stimuli attract visual attention even when task irrelevant, but the consequences of this privileged status for memory are unknown. To address this, we combined computational approaches, eye-tracking methodology, and individual-differences measures. Participants searched for targets in scenes containing social or non-social distracters equated for low-level visual salience. Subsequent memory precision for target locations was tested. Individual differences in autistic symptomatology and social anxiety were also measured. Eye-tracking revealed significantly more attentional capture to social compared to non-social distracters. Critically, memory precision for target locations was poorer for social scenes. This effect was moderated by social anxiety, with anxious individuals remembering target locations better under conditions of social distraction. These findings shed further light onto the privileged attentional status of social stimuli and its functional consequences on memory across individuals