Hippocampal contribution to implicit configuration memory expressed via eye movements during scene exploration

Although hippocampus unequivocally supports explicit/declarative memory, fewer findings have demonstrated its role in implicit expressions of memory. We tested for hippocampal contributions to an implicit expression of configural/relational memory for complex scenes using eye‐movement tracking during functional magnetic resonance imaging (fMRI) scanning. Participants studied scenes and were later tested using scenes that resembled study scenes in their overall feature configuration but comprised different elements. These configurally similar scenes were used to limit explicit memory, and were intermixed with new scenes that did not resemble studied scenes. Scene configuration memory was expressed through eye movements reflecting exploration overlap (EO), which is the viewing of the same scene locations at both study and test. EO reliably discriminated similar study‐test scene pairs from study‐new scene pairs, was reliably greater for similarity‐based recognition hits than for misses, and correlated with hippocampal fMRI activity. In contrast, subjects could not reliably discriminate similar from new scenes by overt judgments, although ratings of familiarity were slightly higher for similar than new scenes. Hippocampal fMRI correlates of this weak explicit memory were distinct from EO‐related activity. These findings collectively suggest that EO was an implicit expression of scene configuration memory associated with hippocampal activity. Visual exploration can therefore reflect implicit hippocampal‐related memory processing that can be observed in eye‐movement behavior during naturalistic scene viewing. © 2015 Wiley Periodicals, Inc.     

Cortical sensitivity to natural scene structure

Natural scenes are inherently structured, with meaningful objects appearing in predictable locations. Human vision is tuned to this structure: When scene structure is purposefully jumbled, perception is strongly impaired. Here, we tested how such perceptual effects are reflected in neural sensitivity to scene structure. During separate fMRI and EEG experiments, participants passively viewed scenes whose spatial structure (i.e., the position of scene parts) and categorical structure (i.e., the content of scene parts) could be intact or jumbled. Using multivariate decoding, we show that spatial (but not categorical) scene structure profoundly impacts on cortical processing: Scene‐selective responses in occipital and parahippocampal cortices (fMRI) and after 255 ms (EEG) accurately differentiated between spatially intact and jumbled scenes. Importantly, this differentiation was more pronounced for upright than for inverted scenes, indicating genuine sensitivity to spatial structure rather than sensitivity to low‐level attributes. Our findings suggest that visual scene analysis is tightly linked to the spatial structure of our natural environments. This link between cortical processing and scene structure may be crucial for rapidly parsing naturalistic visual inputs.     

Entorhinal cortex contributes to object-in-place scene memory

Four rhesus monkeys (Macaca mulatta) were trained preoperatively in a test of object-in-place scene memory. They were presented daily with lists of unique computer-generated scenes each containing a spatial array of multiple individual objects. Within each scene, objects to be discriminated appeared in the foreground, each occupying a unique location, and monkeys were required to correctly discriminate the rewarded object to receive a food reward. Once this preoperative criterion was attained, the monkeys received bilateral entorhinal cortex ablation performed as either one or two surgical operations with a period of testing following each. Postoperatively, they were significantly impaired in learning new object-in-place scene problems. These results show that the entorhinal cortex, like anatomically related structures including the perirhinal cortex and the fornix, contributes to object-in-place scene learning.     

Neurotoxic lesions of ventrolateral prefrontal cortex impair object-in-place scene memory

Disconnection of the frontal lobe from the inferotemporal cortex produces deficits in a number of cognitive tasks that require the application of memory-dependent rules to visual stimuli. The specific regions of frontal cortex that interact with the temporal lobe in performance of these tasks remain undefined. One capacity that is impaired by frontal-temporal disconnection is rapid learning of new object-in-place scene problems, in which visual discriminations between two small typographic characters are learned in the context of different visually complex scenes. In the present study, we examined whether neurotoxic lesions of ventrolateral prefrontal cortex in one hemisphere, combined with ablation of inferior temporal cortex in the contralateral hemisphere, would impair learning of new object-in-place scene problems. Male macaque monkeys learned 10 or 20 new object-in-place problems in each daily test session. Unilateral neurotoxic lesions of ventrolateral prefrontal cortex produced by multiple injections of a mixture of ibotenate and N-methyl-D-aspartate did not affect performance. However, when disconnection from inferotemporal cortex was completed by ablating this region contralateral to the neurotoxic prefrontal lesion, new learning was substantially impaired. Sham disconnection (injecting saline instead of neurotoxin contralateral to the inferotemporal lesion) did not affect performance. These findings support two conclusions: first, that the ventrolateral prefrontal cortex is a critical area within the frontal lobe for scene memory; and second, the effects of ablations of prefrontal cortex can be confidently attributed to the loss of cell bodies within the prefrontal cortex rather than to interruption of fibres of passage through the lesioned area.     

The effect of gaze direction on the different components of visuo-spatial short-term memory

Cerebral asymmetries and cortical regions associated with the upper and lower visual field were investigated using shifts of gaze. Earlier research suggests that gaze shifts to the left or right increase activation of specific areas of the contralateral hemisphere. We asked whether looking at one quadrant of the visual field facilitates the recall in various visuo-spatial tasks. The different components of visuo-spatial memory were investigated by probing memory for a stimulus matrix in each quadrant of the screen. First, memory for visual images or patterns was probed with a matrix of squares that was simultaneously presented and had to be reconstructed by mouse click. Better memory performance was found in the upper left quadrant compared to the three other quadrants indicating that both laterality and elevation are important. Second, positional memory was probed by subsequently presenting squares which prevented the formation of a visual image. Again, we found that gaze to the upper left facilitated performance. Third, memory for object-location binding was probed by asking observers to associate objects to particular locations. Higher performance was found with gaze directed to the lower quadrants irrespective of lateralization, confirming that only some components of visual short-term memory have shared neural substrates.     

Cultural and biological factors modulate spatial biases over development

Increasing evidence supports the contribution of both biological and cultural factors to visuospatial processing. The present study adds to the literature by exploring the interplay of perceptual and linguistic mechanisms in determining visuospatial asymmetries in adults (Experiment 1) and children (Experiment 2). In particular, pre-schoolers (3 and 5 year-olds), school-aged children (8 year-old), and adult participants were required to bisect different types of stimuli, that is, lines, words, and figure strings. In accordance with the literature, results yielded a leftward bias for lines and words and a rightward bias for figure strings, in adult participants. More critically, different biases were found for lines, words, and figure strings in children as a function of age, reflecting the impact of both cultural and biological factors on the processing of different visuospatial materials. Specifically, an adult-like pattern of results emerged only in the older group of children (8 year-old), but not in pre-schoolers. Results are discussed in terms of literacy, reading habits exposure, and biological maturation.     

Hemispheric asymmetries in memory processes as measured in a false recognition paradigm

Although memory differs in important ways between the left and right cerebral hemispheres, the nature of these differences remains controversial. We examined this issue in two experiments using a false memory paradigm that allowed novel tests of two theories that have not been assessed in a common paradigm previously. Lists of semantically related words (e.g., bed, rest, wake…), all highly associated to one “critical” word (e.g., sleep), were presented auditorily during a study phase. Memory for both the related words and the critical words was measured in a subsequent old/new recognition test using divided-visual- field word presentations. The most important results were that the ability to correctly reject previously unpresented words was greater when test items were presented to the right visual field/left hemisphere (RVF/LH) than to the left visual field/right hemisphere (LVF/RH) and that participants were more confident in correctly rejecting unpresented words when test items were presented to the RVF/LH than to the LVF/RH. Results were in line with the theory that associative activation of semantic information is restricted in the left hemisphere but diffuse in the right; however, these results contrasted with the theory that memory traces are interpretive in the left hemisphere but veridical in the right. A potential resolution to the seemingly contradictory theories of asymmetries in memory processing is briefly discussed.     

Differential contributions of the parahippocampal place area and the anterior hippocampus to human memory for scenes

Past neuroimaging research has identified a parahippocampal place area (PPA) in the posterior medial temporal lobe (MTL), which responds preferentially to visual scenes and plays a role in episodic memory for this class of stimuli. In the present positron emission tomography study, we examined to what extent the functional characteristics of the PPA resemble those of other, more anterior MTL regions across various learning and recognition-memory tasks. We also determined whether the involvement of the PPA in recognition of previously studied scenes is specific to a particular type of scene information. We found that, like the PPA, anterior hippocampal regions showed a novelty response (higher activation for novel than repeated scenes) and a stimulus-related response (higher activation for scenes than objects) during learning, indicating that MTL structures other than the PPA contribute to the encoding of novel stimulus relationships in scenes. However, these anterior hippocampal regions showed no involvement during recognition of either spatial or nonspatial information contained in scenes. The PPA, by contrast, was consistently involved in recognition of all types of scene details, presumably through interactions with co-activated parietal and occipitotemporal cortices. We suggest that MTL contributions from the PPA are sufficient to support recognition of scenes when the task can be based on a perceptually based familiarity process.     

Electrophysiological measures of maintaining representations in visual working memory

Visual working memory (WM) is a limited capacity system which maintains information about objects in the immediate visual environment. Recent neurophysiological and neuroimaging studies have identified sustained memory-item specific activity during the retention period of WM tasks, and this activity may be a physiological substrate of maintaining representations in WM. In the present study, we present an electrophysiological measure of delay activity using event-related potentials (ERPs). Subjects were asked to remember the items in a single hemifield presented within a bilateral display. Approximately 200 msec following the onset of the memory array, we observed a large negative wave at electrode sites that were contralateral with respect to the position of the memory items. This activity persisted throughout the retention period and appears to be an analog to delay activity observed in monkey single-unit and functional magnetic resonance imaging (fMRI) WM studies. The contralateral delay activity is modulated by the number of items in the memory array but reaches asymptote for arrays of 3 to 4 items. This activity is similar across different classes of simple objects and the amplitude is smaller on incorrect response trials relative to correct trials, suggesting that this activity is necessary for correct performance on a given trial. Together, these results appear to indicate an electrophysiological index of the maintained representations in visual WM.     

A review of the verbal and visual memory impairments in children with foetal alcohol spectrum disorders

Background: Children with Foetal Alcohol Spectrum Disorders (FASD) have significant impairments in memory, negatively affecting academics and daily functioning.

Primary objective: To review published research on: (1) verbal and visual-spatial memory in children with FASD or prenatal alcohol exposure (PAE); (2) animal research on the impact of PAE on memory; and (3) brain areas involved in memory that are affected by PAE.

Main outcomes: Verbal memory is one of the main areas of memory affected by gestational alcohol exposure, specifically in encoding and retrieving information. Spatial memory has emerged as a dominant deficit in individuals with FASD, consistent in children, adolescents and adults. There are regions of the brain more typically affected by PAE, which have ties to memory functioning. Animal research has confirmed the presence of impacts to key brain regions involved in memory functioning for those affected by PAE.

Conclusion: Memory deficits are a prevalent finding in individuals with PAE. Research in this area is complicated by small sample sizes, difficulty linking animal research to human application and lack of effective connection between existing memory theory and functional memory testing in FASD. New research has shown that there are implications for memory and learning amelioration in children with FASD.     

The human perirhinal cortex and recognition memory

The importance of the perirhinal cortex for visual recognition memory performance is undisputed. However, it has not been clear whether its contribution to performance is mainly perceptual, or mainly mnemonic, or whether the perirhinal cortex contributes to both perception and memory. We determined the effects of medial temporal lobe damage that includes complete damage to the perirhinal cortex in two amnesic patients by assessing recognition memory for complex visual stimuli across delays from 0 to 40 s. These patients, as well as six other amnesic patients with damage limited to the hippocampal formation or diencephalic structures, exhibited intact recognition memory at delays of 0–2 s and a delay-dependent memory impairment at delays of 6 s and longer. Additionally, the patients with damage to the perirhinal cortex performed worse than the other amnesic patients at delays of 25 s and longer. The findings suggest that the perirhinal cortex is not important for visual perception or immediate memory. In this respect, the findings for perirhinal cortex resemble the findings for other medial temporal lobe structures, including the hippocampus. Hippocampus 1998;8:330–339. © 1998 Wiley-Liss, Inc.     

Visual learning and memory as functions of age

Age-related changes have been reported for a range of perceptual and cognitive functions. We investigated visual acuity and vernier acuity, as well as visual memory and learning, in four age groups, each comprising 10 subjects and ranging from adolescence to an age group up to 66 years. The groups were matched on general abilities for visuospatial information processing. Visual acuity decreased slightly with increasing age. The reproduction of more complex geometrical material which exceeded short-term memory capacities was significantly impaired in the oldest group relative to young adults. However, vernier acuity thresholds and improvement of thresholds with training did not differ in the four groups. Short-term retention of visual stimuli across 1 or 4 sec was also comparable in the different age groups. Those visual abilities that are limited primarily by cortical, not retinal, factors remained relatively unchanged in our observers despite age-related changes in the eye. Visual memory functions which tap working and long-term memory abilities, on the other hand, showed a significant age-associated decline during adulthood.     

Selective memory impairment for personally familiar colors following encephalitis

A 19-year-old man presented with a peculiar memory impairment following non-herpetic viral encephalitis. He was exclusively impaired in generating images for colors of possessions previously well known to him, and consequently these seemed less familiar. He appeared unable to access personally familiar and autobiographical color attributes. Single-photon emission computed tomography and electroencephalogram findings suggest that the right-sided functional abnormalities, specifically in the frontal and temporal regions, were implicated as the functional locus for the patient's unique problem.     

Preserved visual recognition memory in an amnesic patient with hippocampal lesions

There is ongoing debate about whether performance on tests of recognition memory can remain preserved after hippocampal damage. In the present study, we report F.R.G., a patient who became severely amnesic following herpes simplex encephalitis. Although F.R.G. failed all tests involving recall and verbal recognition, she obtained normal performance on a wide number of tests evaluating visual recognition memory (14 of 18 different tests). Her performance was independent of various factors, such as test difficulty, duration of exposure to the stimuli, or delay separating encoding and recognition. F.R.G. also achieved normal performance on two tasks requiring that she associate pairs of visual stimuli. In addition, she demonstrated spared feeling of knowing, suggesting that her performance on recognition tests was explicit and likely to rely on familiarity. Brain imaging (MRI) revealed bilateral lesions of the hippocampus and lesions of the left parahippocampal gyrus, while the right parahippocampal gyrus remained relatively spared. The results of this study support the view that recognition memory can be preserved despite severe hippocampal damage and that familiarity is a distinct memory process that can be dissociated from recollection.     

Visual half-field testing of memory functions in patients considered for surgical treatment of intractable complex partial epilepsy

The present research employed the visual half-field (VHF) technique to assess memory functions in normal subjects and in patients with unilateral temporal lobe epilepsy prior to surgery. Two studies were conducted. In Study 1, concrete and abstract words were presented to the left (LVF) or the right visual half field (RVF), and measures were made of response latencies, naming, free recall, and recognition. In Study 2, pictures depicting random shapes with low verbal association values were presented, and measures were made of latencies for identification and recognition of the shapes. Overall, the results showed a RVF advantage for words, but no lateralization for shapes. A selective hemisphere memory deficit was obtained for abstract words in patients with left temporal lobe lesions. Otherwise, no obvious lesion-related differences were found in the preoperative analyses. It is concluded that VHF testing of verbal information, but not abstract visuo-spatial information, is discriminative in assessing hemispheric functions in normal subjects and patients with temporal-lobe epileptic lesions.     

Same task,different strategies: How brain networks can be influenced by memory strategy

Previous functional neuroimaging studies demonstrated that different neural networks underlie different types of cognitive processing by engaging participants in particular tasks, such as verbal or spatial working memory (WM) tasks. However, we report here that even when a WM task is defined as verbal or spatial, different types of memory strategies may be used to complete it, with concomitant variations in brain activity. We developed a questionnaire to characterize the type of strategy used by individual members in a group of 28 young healthy participants (18–25 years) during a spatial WM task. A cluster analysis was performed to differentiate groups. We acquired functional magnetoencephalography and structural diffusion tensor imaging measures to characterize the brain networks associated with the use of different strategies. We found two types of strategies were used during the spatial WM task, a visuospatial and a verbal strategy, and brain regions and time courses of activation differed between participants who used each. Task performance also varied by type of strategy used with verbal strategies showing an advantage. In addition, performance on neuropsychological tests (indices from Wechsler Adult Intelligence Scale‐IV, Rey Complex Figure Test) correlated significantly with fractional anisotropy measures for the visuospatial strategy group in white matter tracts implicated in other WM and attention studies. We conclude that differences in memory strategy can have a pronounced effect on the locations and timing of brain activation and that these differences need further investigation as a possible confounding factor for studies using group averaging as a means for summarizing results. Hum Brain Mapp 35:5127–5140, 2014. © 2014 Wiley Periodicals, Inc .     

Prefrontal oxygenation during working memory in ADHD

Objectives

Deficits in working memory have been repeatedly found on a behavioural level in children with attention-deficit/hyperactivity disorder (ADHD). Functional brain imaging studies have revealed evidence for alterations in the prefrontal cortex associated with working memory. So far it remains unresolved whether object (OWM) and spatial visual working memory (SWM) are distinctly impaired in ADHD. We investigated this issue with the fist multi-channel functional near-infrared spectroscopy study of children with ADHD.

Method

We investigated 19 children with ADHD combined type (DSM-IV) and 19 controls matched for age (8-15 years), sex, handedness, and intelligence during a working memory task assessing OWM and SWM separately, and a control condition (CON). Prefrontal brain activity was measured by concentration changes of oxygenated haemoglobin.

Results

Working memory performance showed significant differences for conditions (OWM > SWM > CON), but no differences between groups. Cortical prefrontal activation was significantly higher for OWM and SWM in contrast to CON, again with no differences between groups.

Conclusions

We found no indication for an altered prefrontal processing during OWM and SWM tasks in ADHD children compared to controls. Reviewing the existing imaging literature on working memory in ADHD and considering the present data, we discuss possible confounding factors relevant for brain activity in previous, the current, and future investigations. Thus, it is of high importance to capture developmental trajectories, task specific discrepancies, and effects of permanent medication intake in future studies.     

Reduced performance in tests of memory and visual abstraction in seamen exposed to industrial solvents

Eighty-five seamen exposed to a variety of organic solvents and hydrocarbon compounds during their work on chemical tankers were compared with 59 unexposed seamen. Visual memory, auditory memory and visual abstraction were examined 14 days or more after the last solvent exposure. Multivariate analyses were performed to control the effects of confounding factors such as age, alcohol consumption, smoking, cerebral concussions and educational level. Significant correlations were found between increasing solvent exposure and poor results in tests of auditory memory and visual abstraction. These results indicate adverse psychological effects caused by chronic organic solvent exposure.     

The neuropsychology of autobiographical memory

This special issue of Cortex focuses on the relative contribution of different neural networks to memory and the interaction of ‘core' memory processes with other cognitive processes. In this article, we examine both. Specifically, we identify cognitive processes other than encoding and retrieval that are thought to be involved in memory; we then examine the consequences of damage to brain regions that support these processes. This approach forces a consideration of the roles of brain regions outside of the frontal, medial- temporal, and diencephalic regions that form a central part of neurobiological theories of memory. Certain kinds of damage to visual cortex or lateral temporal cortex produced impairments of visual imagery or semantic memory; these patterns of impairment are associated with a unique pattern of amnesia that was distinctly different from the pattern associated with medial-temporal trauma. On the other hand, damage to language regions, auditory cortex, or parietal cortex produced impairments of language, auditory imagery, or spatial imagery; however, these impairments were not associated with amnesia. Therefore, a full model of autobiographical memory must consider cognitive processes that are not generally considered ‘core processes,' as well as the brain regions upon which these processes depend.