Deployment of Spatial Attention towards Locations in Memory Representations. An EEG Study

Recalling information from visual short-term memory (VSTM) involves the same neural mechanisms as attending to an actually perceived scene. In particular, retrieval from VSTM has been associated with orienting of visual attention towards a location within a spatially-organized memory representation. However, an open question concerns whether spatial attention is also recruited during VSTM retrieval even when performing the task does not require access to spatial coordinates of items in the memorized scene. The present study combined a visual search task with a modified, delayed central probe protocol, together with EEG analysis, to answer this question. We found a temporal contralateral negativity (TCN) elicited by a centrally presented go-signal which was spatially uninformative and featurally unrelated to the search target and informed participants only about a response key that they had to press to indicate a prepared target-present vs. -absent decision. This lateralization during VSTM retrieval (TCN) provides strong evidence of a shift of attention towards the target location in the memory representation, which occurred despite the fact that the present task required no spatial (or featural) information from the search to be encoded, maintained, and retrieved to produce the correct response and that the go-signal did not itself specify any information relating to the location and defining feature of the target.     

Neural mechanisms of human perceptual learning: electrophysiological evidence for a two-stage process

Background

Humans and other animals change the way they perceive the world due to experience. This process has been labeled as perceptual learning, and implies that adult nervous systems can adaptively modify the way in which they process sensory stimulation. However, the mechanisms by which the brain modifies this capacity have not been sufficiently analyzed.

Methodology/Principal Findings

We studied the neural mechanisms of human perceptual learning by combining electroencephalographic (EEG) recordings of brain activity and the assessment of psychophysical performance during training in a visual search task. All participants improved their perceptual performance as reflected by an increase in sensitivity (d'') and a decrease in reaction time. The EEG signal was acquired throughout the entire experiment revealing amplitude increments, specific and unspecific to the trained stimulus, in event-related potential (ERP) components N2pc and P3 respectively. P3 unspecific modification can be related to context or task-based learning, while N2pc may be reflecting a more specific attentional-related boosting of target detection. Moreover, bell and U-shaped profiles of oscillatory brain activity in gamma (30–60 Hz) and alpha (8–14 Hz) frequency bands may suggest the existence of two phases for learning acquisition, which can be understood as distinctive optimization mechanisms in stimulus processing.

Conclusions/Significance

We conclude that there are reorganizations in several neural processes that contribute differently to perceptual learning in a visual search task. We propose an integrative model of neural activity reorganization, whereby perceptual learning takes place as a two-stage phenomenon including perceptual, attentional and contextual processes.     

Learning in simple systems

Cellular processes that mediate learning and memory show a remarkable level of conservation between vertebrates and invertebrates. Recent studies have shown that learning and memory formation in invertebrates, so-called 'simple systems', involves a highly complex arrangement of cellular pathways. Some pathways contribute to a single stage of memory formation, whereas others impact on multiple stages of memory development. Distinct cellular pathways may also act in series or in parallel during various stages of memory formation.     

Reward-Priming of Location in Visual Search

Existing visual search research has demonstrated that the receipt of reward will be beneficial for subsequent perceptual and attentional processing of features that have characterized targets, but detrimental for processing of features that have characterized irrelevant distractors. Here we report a similar effect of reward on location. Observers completed a visual search task in which they selected a target, ignored a salient distractor, and received random-magnitude reward for correct performance. Results show that when target selection garnered rewarding outcome attention is subsequently a.) primed to return to the target location, and b.) biased away from the location that was occupied by the salient, task-irrelevant distractor. These results suggest that in addition to priming features, reward acts to guide visual search by priming contextual locations of visual stimuli.     

Operant visual learning and memory in Drosophila mutants dunce,amnesiac and radish

Learning and memory of Drosophila mutants dunce, amnesiac and radish which were isolated originally from the classical olfactory learning paradigm are analyzed in an operant visual learning paradigm. Dunce appears to show normal ability to learn during training, but its memory is significantly affected. Though the learning index during the first minute after training is normal, its short-term memory (STM), anesthesia-resistant memory (ARM) and long-term memory (LTM) are all significantly damaged. Amnesiac displays disrupted middle-term memory (MTM), while its STM and LTM remain unchanged. Learning and memory in radish mutants seem to be unaffected. These results lend support to the argument that there are certain common molecular mechanisms underlying learning and memory through different tasks and the previous multi-phase model of visual memory is modified in a genetic way.     

Ganzfeld Stimulation or Sleep Enhance Long Term Motor Memory Consolidation Compared to Normal Viewing in Saccadic Adaptation Paradigm

Adaptation of saccade amplitude in response to intra-saccadic target displacement is a type of implicit motor learning which is required to compensate for physiological changes in saccade performance. Once established trials without intra-saccadic target displacement lead to de-adaptation or extinction, which has been attributed either to extra-retinal mechanisms of spatial constancy or to the influence of the stable visual surroundings. Therefore we investigated whether visual deprivation (“Ganzfeld”-stimulation or sleep) can partially maintain this motor learning compared to free viewing of the natural surroundings. Thirty-five healthy volunteers performed two adaptation blocks of 100 inward adaptation trials – interspersed by an extinction block – which were followed by a two-hour break with or without visual deprivation (VD). Using additional adaptation and extinction blocks short and long (4 weeks) term memory of this implicit motor learning were tested. In the short term, motor memory tested immediately after free viewing was superior to adaptation performance after VD. In the long run, however, effects were opposite: motor memory and relearning of adaptation was superior in the VD conditions. This could imply independent mechanisms that underlie the short-term ability of retrieving learned saccadic gain and its long term consolidation. We suggest that subjects mainly rely on visual cues (i.e., retinal error) in the free viewing condition which makes them prone to changes of the visual stimulus in the extinction block. This indicates the role of a stable visual array for resetting adapted saccade amplitudes. In contrast, visual deprivation (GS and sleep), might train subjects to rely on extra-retinal cues, e.g., efference copy or prediction to remap their internal representations of saccade targets, thus leading to better consolidation of saccadic adaptation.     

A slowing effect on visual search by advance information in pigeons (Columba livia): a comparison with humans (Homo sapiens)

A comparative study was conducted to investigate whether the search for a target letter was facilitated when the target and prime (preceding stimulus) letters were identical. Pigeons (Section 2) and human participants (Section 3) were first trained to search for “A” among “Y”s and “E” among “D”s in a condition in which a square shape appeared as the prime (Neutral condition). In subsequent testing, a prime was identical either to the corresponding target (Target-priming condition) or to the distractor (Distractor-priming condition). Humans and pigeons responded differently to the two priming conditions. On early trials, the Target prime facilitated search in humans, reducing reaction times (RTs) to targets. In pigeons, however, RTs were longer with Target primes, suggesting that pre-exposure to target letters may directly inhibit the search for targets in subsequent search displays. Furthermore, pre-exposure to the distractor letters may inhibit the processing of the distractor. On later trials, RTs of humans were faster in both priming conditions than in the Neutral condition, suggesting that expectation of a target facilitated search (“Y” predicted “A” and “D” predicted “E”). In contrast, the pigeons showed no evidence of expectation-based facilitation, with constant slowing effects of the Target prime extending across sessions. Possible mechanisms underlying such a slowing priming effect in pigeons were discussed.     

Memory,consciousness and neuroimaging.

Neuroimaging techniques that allow the assessment of memory performance in healthy human volunteers while simultaneously obtaining measurements of brain activity in vivo may offer new information on the neural correlates of particular forms of memory retrieval and their association with consciousness and intention. We consider evidence from studies with positron emission tomography and functional magnetic resonance imaging indicating that priming, a form of implicit retrieval, is associated with decreased activity in various cortical regions. We also consider evidence concerning the question of whether two components of explicit retrieval--intentional or effortful search and successful conscious recollection--are preferentially associated with increased activity in prefrontal and medial temporal regions, respectively. Last, we consider recent efforts to probe the relation between the phenomenological character of remembering and neural activity. In this instance we broaden our scope to include studies employing event-related potentials and consider evidence concerning the neural correlates of qualitatively different forms of memory, including memory that is specifically associated with a sense of self, and the recollection of particular temporal or perceptual features that might contribute to a rich and vivid experience of the past.     

Early genomics of learning and memory: a review

The characterization of the molecular mechanisms whereby our brain codes, stores and retrieves memories remains a fundamental puzzle in neuroscience. Despite the knowledge that memory storage involves gene induction, the identification and characterization of the effector genes has remained elusive. The completion of the Human Genome Project and a variety of new technologies are revolutionizing the way these mechanisms can be explored. This review will examine how a genomic approach can be used to dissect and analyze the complex dynamic interactions involved in gene regulation during learning and memory. This innovative approach is providing information on a new class of genes associated with learning and memory in health and disease and is elucidating new molecular targets and pathways whose pharmacological modulation may allow new therapeutic approaches for improving cognition.     

Age‐related changes in hippocampal‐dependent synaptic plasticity and memory mediated by p75 neurotrophin receptor

The plasticity mechanisms in the nervous system that are important for learning and memory are greatly impacted during aging. Notably, hippocampal‐dependent long‐term plasticity and its associative plasticity, such as synaptic tagging and capture (STC), show considerable age‐related decline. The p75 neurotrophin receptor (p75^NTR) is a negative regulator of structural and functional plasticity in the brain and thus represents a potential candidate to mediate age‐related alterations. However, the mechanisms by which p75^NTR affects synaptic plasticity of aged neuronal networks and ultimately contribute to deficits in cognitive function have not been well characterized. Here, we report that mutant mice lacking the p75^NTR were resistant to age‐associated changes in long‐term plasticity, associative plasticity, and associative memory. Our study shows that p75^NTR is responsible for age‐dependent disruption of hippocampal homeostatic plasticity by modulating several signaling pathways, including BDNF, MAPK, Arc, and RhoA‐ROCK2‐LIMK1‐cofilin. p75^NTR may thus represent an important therapeutic target for limiting the age‐related memory and cognitive function deficits.     

Use of spatial information and search strategies in a water maze analog in Drosophila melanogaster

Learning the spatial organization of the environment is crucial to fitness in most animal species. Understanding proximate and ultimate factors underpinning spatial memory is thus a major goal in the study of animal behavior. Despite considerable interest in various aspects of its behavior and biology, the model species Drosophila melanogaster lacks a standardized apparatus to investigate spatial learning and memory. We propose here a novel apparatus, the heat maze, conceptually based on the Morris water maze used in rodents. Using the heat maze, we demonstrate that D. melanogaster flies are able to use either proximal or distal visual cues to increase their performance in navigating to a safe zone. We also show that flies are actively using the orientation of distal visual cues when relevant in targeting the safe zone, i.e., Drosophila display spatial learning. Parameter-based classification of search strategies demonstrated the progressive use of spatially precise search strategies during learning. We discuss the opportunity to unravel the mechanistic and evolutionary bases of spatial learning in Drosophila using the heat maze.     

Sleep-Effects on Implicit and Explicit Memory in Repeated Visual Search

In repeated visual search tasks, facilitation of reaction times (RTs) due to repetition of the spatial arrangement of items occurs independently of RT facilitation due to improvements in general task performance. Whereas the latter represents typical procedural learning, the former is a kind of implicit memory that depends on the medial temporal lobe (MTL) memory system and is impaired in patients with amnesia. A third type of memory that develops during visual search is the observers’ explicit knowledge of repeated displays. Here, we used a visual search task to investigate whether procedural memory, implicit contextual cueing, and explicit knowledge of repeated configurations, which all arise independently from the same set of stimuli, are influenced by sleep. Observers participated in two experimental sessions, separated by either a nap or a controlled rest period. In each of the two sessions, they performed a visual search task in combination with an explicit recognition task. We found that (1) across sessions, MTL-independent procedural learning was more pronounced for the nap than rest group. This confirms earlier findings, albeit from different motor and perceptual tasks, showing that procedural memory can benefit from sleep. (2) Likewise, the sleep group compared with the rest group showed enhanced context-dependent configural learning in the second session. This is a novel finding, indicating that the MTL-dependent, implicit memory underlying contextual cueing is also sleep-dependent. (3) By contrast, sleep and wake groups displayed equivalent improvements in explicit recognition memory in the second session. Overall, the current study shows that sleep affects MTL-dependent as well as MTL-independent memory, but it affects different, albeit simultaneously acquired, forms of MTL-dependent memory differentially.     

Problems of learning and memory: one or multiple memory systems?

Learning, and hence memory, is ubiquitous not only throughout the animal kingdom, but apparently throughout many regions of the brain. Is all learning reducible to a single common form? Neuropsychological dissociations suggest that the mammalian brain possesses a number of different and potentially independent memory systems, with different mechanisms and anatomical dispositions, some of which are neurally widely dispersed and others of which are narrowly organized. Among the types considered are: (i) short-term memory; (ii) knowledge and skills; (iii) stable associative memory; (iv) event memory; and (v) priming. As double or multiple dissociations do not lead to logically inevitable conclusions, it has been argued that an alternative to multiple memory systems is variable modes of processing. But these, too, would be dissociable on the same lines of evidence. Dissociations, if strong and absolute, have strong pragmatic power when they are combined with evolutionary and neuroscientific evidence. Multiple memory systems may possibly share some common cellular mechanisms, but such mechanisms do not define the separate properties at the systems level.     

Semantic integration by pattern priming: experiment and cortical network model

Neural network models describe semantic priming effects by way of mechanisms of activation of neurons coding for words that rely strongly on synaptic efficacies between pairs of neurons. Biologically inspired Hebbian learning defines efficacy values as a function of the activity of pre- and post-synaptic neurons only. It generates only pair associations between words in the semantic network. However, the statistical analysis of large text databases points to the frequent occurrence not only of pairs of words (e.g., “the way”) but also of patterns of more than two words (e.g., “by the way”). The learning of these frequent patterns of words is not reducible to associations between pairs of words but must take into account the higher level of coding of three-word patterns. The processing and learning of pattern of words challenges classical Hebbian learning algorithms used in biologically inspired models of priming. The aim of the present study was to test the effects of patterns on the semantic processing of words and to investigate how an inter-synaptic learning algorithm succeeds at reproducing the experimental data. The experiment manipulates the frequency of occurrence of patterns of three words in a multiple-paradigm protocol. Results show for the first time that target words benefit more priming when embedded in a pattern with the two primes than when only associated with each prime in pairs. A biologically inspired inter-synaptic learning algorithm is tested that potentiates synapses as a function of the activation of more than two pre- and post-synaptic neurons. Simulations show that the network can learn patterns of three words to reproduce the experimental results.     

Reductions in cortical activity during priming

Priming is a nonconscious form of memory in which an encounter with a stimulus influences the subsequent identification, production or classification of the same or a related stimulus. Neuroimaging studies have revealed that behavioral priming is typically accompanied by reduced activity in several cortical regions. We review recent studies that have concerned two key issues. First, specificity effects produced by changes between study and test in either the physical features of stimuli or the behavioral response reveal cortical sensitivity to the perceptual, conceptual and stimulus-to-decision mapping properties of primed items. Second, correlations between behavioral priming and activity reductions are robust across a range of tasks and procedures in prefrontal regions but not in posterior regions. On the basis of these recent studies, we suggest that the reduction in cortical activity during priming involves at least two different mechanisms.     

Sex differences in search and gathering skills

The hunter–gatherer theory of sex differences states that female cognition has evolutionarily adapted to gathering and male cognition to hunting. Existing studies corroborate that men excel in hunting-related skills, but there is only indirect support for women excelling in gathering tasks. This study tested if women would outperform men in laboratory-based computer tests of search and gathering skills. In Experiment 1, men found target objects faster and made fewer mistakes than women in a classic visual search study. In Experiment 2, participants gathered items (fruits or letters presented on screen), and again, men performed significantly better. In Experiment 3, participants' incidental learning of object locations in a search experiment was studied, but no statistically significant sex differences were observed. These findings found the opposite of what was expected based on the hypothesis that female cognition has adapted to gathering. Alternative interpretations of the role of object location memory, female gathering roles and the division of labor between the sexes are discussed.     

Impaired Contingent Attentional Capture Predicts Reduced Working Memory Capacity in Schizophrenia

Although impairments in working memory (WM) are well documented in schizophrenia, the specific factors that cause these deficits are poorly understood. In this study, we hypothesized that a heightened susceptibility to attentional capture at an early stage of visual processing would result in working memory encoding problems. 30 patients with schizophrenia and 28 demographically matched healthy participants were presented with a search array and asked to report the orientation of the target stimulus. In some of the trials, a flanker stimulus preceded the search array that either matched the color of the target (relevant-flanker capture) or appeared in a different color (irrelevant-flanker capture). Working memory capacity was determined in each individual using the visual change detection paradigm. Patients needed considerably more time to find the target in the no-flanker condition. After adjusting the individual exposure time, both groups showed equivalent capture costs in the irrelevant-flanker condition. However, in the relevant-flanker condition, capture costs were increased in patients compared to controls when the stimulus onset asynchrony between the flanker and the search array was high. Moreover, the increase in relevant capture costs correlated negatively with working memory capacity. This study demonstrates preserved stimulus-driven attentional capture but impaired contingent attentional capture associated with low working memory capacity in schizophrenia. These findings suggest a selective impairment of top-down attentional control in schizophrenia, which may impair working memory encoding.     

Roles of NO Signaling in Long-Term Memory Formation in Visual Learning in an Insect

Many insects exhibit excellent capability of visual learning, but the molecular and neural mechanisms are poorly understood. This is in contrast to accumulation of information on molecular and neural mechanisms of olfactory learning in insects. In olfactory learning in insects, it has been shown that cyclic AMP (cAMP) signaling critically participates in the formation of protein synthesis-dependent long-term memory (LTM) and, in some insects, nitric oxide (NO)-cyclic GMP (cGMP) signaling also plays roles in LTM formation. In this study, we examined the possible contribution of NO-cGMP signaling and cAMP signaling to LTM formation in visual pattern learning in crickets. Crickets that had been subjected to 8-trial conditioning to associate a visual pattern with water reward exhibited memory retention 1 day after conditioning, whereas those subjected to 4-trial conditioning exhibited 30-min memory retention but not 1-day retention. Injection of cycloheximide, a protein synthesis inhibitor, into the hemolymph prior to 8-trial conditioning blocked formation of 1-day memory, whereas it had no effect on 30-min memory formation, indicating that 1-day memory can be characterized as protein synthesis-dependent long-term memory (LTM). Injection of an inhibitor of the enzyme producing an NO or cAMP prior to 8-trial visual conditioning blocked LTM formation, whereas it had no effect on 30-min memory formation. Moreover, injection of an NO donor, cGMP analogue or cAMP analogue prior to 4-trial conditioning induced LTM. Induction of LTM by an NO donor was blocked by DDA, an inhibitor of adenylyl cyclase, an enzyme producing cAMP, but LTM induction by a cAMP analogue was not impaired by L-NAME, an inhibitor of NO synthase. The results indicate that cAMP signaling is downstream of NO signaling for visual LTM formation. We conclude that visual learning and olfactory learning share common biochemical cascades for LTM formation.     

Feature-based attention: it is all bottom-up priming

Feature-based attention (FBA) enhances the representation of image characteristics throughout the visual field, a mechanism that is particularly useful when searching for a specific stimulus feature. Even though most theories of visual search implicitly or explicitly assume that FBA is under top-down control, we argue that the role of top-down processing in FBA may be limited. Our review of the literature indicates that all behavioural and neuro-imaging studies investigating FBA suffer from the shortcoming that they cannot rule out an effect of priming. The mere attending to a feature enhances the mandatory processing of that feature across the visual field, an effect that is likely to occur in an automatic, bottom-up way. Studies that have investigated the feasibility of FBA by means of cueing paradigms suggest that the role of top-down processing in FBA is limited (e.g. prepare for red). Instead, the actual processing of the stimulus is needed to cause the mandatory tuning of responses throughout the visual field. We conclude that it is likely that all FBA effects reported previously are the result of bottom-up priming.