Implicit associative learning engages the hippocampus and interacts with explicit associative learning

The hippocampus is crucial for conscious, explicit memory, but whether it is also involved in nonconscious, implicit memory is uncertain. We investigated with functional magnetic resonance imaging whether implicit learning engages the hippocampus and interacts with subsequent explicit learning. The presentation of subliminal faces-written profession pairs for implicit learning was followed by the explicit learning of supraliminal pairs composed of the same faces combined with written professions semantically incongruous to those presented subliminally (experiment 1), semantically congruous professions (experiment 2), or identical professions (experiment 3). We found that implicit face-profession learning interacted with explicit face-profession learning in all experiments, impairing the explicit retrieval of the associations. Hippocampal activity increased during the subliminal presentation of face-profession pairs versus face-nonword pairs and correlated with the later impairment of explicit retrieval. These findings suggest that implicit semantic associative learning engages the hippocampus and influences explicit memory.     

Effects of unconscious processing on implicit memory for fearful faces

Emotional stimuli can be processed even when participants perceive them without conscious awareness, but the extent to which unconsciously processed emotional stimuli influence implicit memory after short and long delays is not fully understood. We addressed this issue by measuring a subliminal affective priming effect in Experiment 1 and a long-term priming effect in Experiment 2. In Experiment 1, a flashed fearful or neutral face masked by a scrambled face was presented three times, then a target face (either fearful or neutral) was presented and participants were asked to make a fearful/neutral judgment. We found that, relative to a neutral prime face (neutral-fear face), a fearful prime face speeded up participants' reaction to a fearful target (fear-fear face), when they were not aware of the masked prime face. But this response pattern did not apply to the neutral target. In Experiment 2, participants were first presented with a masked faces six times during encoding. Three minutes later, they were asked to make a fearful/neutral judgment for the same face with congruent expression, the same face with incongruent expression or a new face. Participants showed a significant priming effect for the fearful faces but not for the neutral faces, regardless of their awareness of the masked faces during encoding. These results provided evidence that unconsciously processed stimuli could enhance emotional memory after both short and long delays. It indicates that emotion can enhance memory processing whether the stimuli are encoded consciously or unconsciously.     

Neural manifestations of memory with and without awareness

Neurophysiological events responsible for different types of human memory tend to occur concurrently and are therefore difficult to measure independently. To surmount this problem, we produced perceptual priming (indicated by speeded responses) in the absence of conscious remembering. At encoding, faces appeared briefly while subjects' attention was diverted to other stimuli. Faces appeared again in either an implicit or explicit memory test. Neural correlates of priming were identified as brain potentials beginning 270 ms after face onset with more negative amplitudes for repeated than for new faces. Remembered faces, in contrast, activated a different configuration of intracranial sources producing positive potentials maximal at 600-700 ms. We thus disentangled and characterized distinct neural events associated with memory with and without awareness.     

Eye Movements Index Implicit Memory Expression in Fear Conditioning

The role of contingency awareness in simple associative learning experiments with human participants is currently debated. Since prior work suggests that eye movements can index mnemonic processes that occur without awareness, we used eye tracking to better understand the role of awareness in learning aversive Pavlovian conditioning. A complex real-world scene containing four embedded household items was presented to participants while skin conductance, eye movements, and pupil size were recorded. One item embedded in the scene served as the conditional stimulus (CS). One exemplar of that item (e.g. a white pot) was paired with shock 100 percent of the time (CS+) while a second exemplar (e.g. a gray pot) was never paired with shock (CS-). The remaining items were paired with shock on half of the trials. Participants rated their expectation of receiving a shock during each trial, and these expectancy ratings were used to identify when (i.e. on what trial) each participant became aware of the programmed contingencies. Disproportionate viewing of the CS was found both before and after explicit contingency awareness, and patterns of viewing distinguished the CS+ from the CS-. These observations are consistent with “dual process” models of fear conditioning, as they indicate that learning can be expressed in patterns of viewing prior to explicit contingency awareness.     

Seeing emotion with your ears: emotional prosody implicitly guides visual attention to faces

Interpersonal communication involves the processing of multimodal emotional cues, particularly facial expressions (visual modality) and emotional speech prosody (auditory modality) which can interact during information processing. Here, we investigated whether the implicit processing of emotional prosody systematically influences gaze behavior to facial expressions of emotion. We analyzed the eye movements of 31 participants as they scanned a visual array of four emotional faces portraying fear, anger, happiness, and neutrality, while listening to an emotionally-inflected pseudo-utterance (Someone migged the pazing) uttered in a congruent or incongruent tone. Participants heard the emotional utterance during the first 1250 milliseconds of a five-second visual array and then performed an immediate recall decision about the face they had just seen. The frequency and duration of first saccades and of total looks in three temporal windows ([0-1250 ms], [1250-2500 ms], [2500-5000 ms]) were analyzed according to the emotional content of faces and voices. Results showed that participants looked longer and more frequently at faces that matched the prosody in all three time windows (emotion congruency effect), although this effect was often emotion-specific (with greatest effects for fear). Effects of prosody on visual attention to faces persisted over time and could be detected long after the auditory information was no longer present. These data imply that emotional prosody is processed automatically during communication and that these cues play a critical role in how humans respond to related visual cues in the environment, such as facial expressions.     

A paradoxical role for inhibition in initiation

Subliminal stimuli, of which subjects are unaware, affect movements made to subsequent visible cues. Sumner and colleagues in this issue of Neuron show that restricted supplementary motor and eye field lesions compromise voluntary control of action because they disrupt the normal unconscious and automatic inhibition of alternative movements partially activated by subliminal stimuli.     

Modulation of Self-Esteem in Self- and Other-Evaluations Primed by Subliminal and Supraliminal Faces

Background

Past research examining implicit self-evaluation often manipulated self-processing as task-irrelevant but presented self-related stimuli supraliminally. Even when tested with more indirect methods, such as the masked priming paradigm, participants'' responses may still be subject to conscious interference. Our study primed participants with either their own or someone else''s face, and adopted a new paradigm to actualize strict face-suppression to examine participants'' subliminal self-evaluation. In addition, we investigated how self-esteem modulates one''s implicit self-evaluation and validated the role of awareness in creating the discrepancy on past findings between measures of implicit self-evaluation and explicit self-esteem.

Methodology/Principal Findings

Participants'' own face or others'' faces were subliminally presented with a Continuous Flash Suppression (CFS) paradigm in Experiment 1, but supraliminally presented in Experiment 2, followed by a valence judgment task of personality adjectives. Participants also completed the Rosenberg Self-Esteem Scale in each experiment. Results from Experiment 1 showed a typical bias of self-positivity among participants with higher self-esteem, but only a marginal self-positivity bias and a significant other-positivity bias among those with lower self-esteem. However, self-esteem had no modulating effect in Experiment 2: All participants showed the self-positivity bias.

Conclusions/Significance

Our results provide direct evidence that self-evaluation manifests in different ways as a function of awareness between individuals with different self-views: People high and low in self-esteem may demonstrate different automatic reactions in the subliminal evaluations of the self and others; but the involvement of consciousness with supraliminally presented stimuli may reduce this dissociation.     

Interpreting local visual features as a global shape requires awareness

How the brain constructs a coherent representation of the environment from noisy visual input remains poorly understood. Here, we explored whether awareness of the stimulus plays a role in the integration of local features into a representation of global shape. Participants were primed with a shape defined either by position or orientation cues, and performed a shape-discrimination task on a subsequently presented probe shape. Crucially, the probe could either be defined by the same or different cues as the prime, which allowed us to distinguish the effect of priming by local features and global shape. We found a robust priming benefit for visible primes, with response times being faster when the probe and prime were the same shape, regardless of the defining cue. However, rendering the prime invisible uncovered a dissociation: position-defined primes produced behavioural benefit only for probes of the same cue type. Surprisingly, orientation-defined primes afforded an enhancement only for probes of the opposite cue. In further experiments, we showed that the effect of priming was confined to retinotopic coordinates and that there was no priming effect by invisible orientation cues in an orientation-discrimination task. This explains the absence of priming by the same cue in our shape-discrimination task. In summary, our findings show that while in the absence of awareness orientation signals can recruit retinotopic circuits (e.g. intrinsic lateral connections), conscious processing is necessary to interpret local features as global shape.     

Human implicit memory for irrelevant dimension values is similar to rats' incidental memory in simultaneous discrimination tasks

Participants completed a category-learning task in which they needed to discover which of three stimulus dimensions (shape, color or size) was relevant. After meeting a learning criterion (nine of 10 consecutive correct responses), participants continued making categorization choices and response latencies associated with these trials were examined. In both Experiments 1 and 2, people responded reliably faster when correct responses matched the previous responses with respect to irrelevant dimension values. Thus, they demonstrated a form of incidental short-term memory analogous to that we previously reported in studies of rats. In Experiment 2, participants' explicit memory for irrelevant dimension values was assessed after category learning was complete. The results indicated that people were unaware of the irrelevant dimension values encountered on trials preceding surprise probe trials. This indicates that memory for the irrelevant dimension values was implicit (i.e. unconscious). The findings are discussed with respect to both human and non-human studies of hippocampus-independent memory and implicit memory.     

Looking the part: social status cues shape race perception

It is commonly believed that race is perceived through another's facial features, such as skin color. In the present research, we demonstrate that cues to social status that often surround a face systematically change the perception of its race. Participants categorized the race of faces that varied along White-Black morph continua and that were presented with high-status or low-status attire. Low-status attire increased the likelihood of categorization as Black, whereas high-status attire increased the likelihood of categorization as White; and this influence grew stronger as race became more ambiguous (Experiment 1). When faces with high-status attire were categorized as Black or faces with low-status attire were categorized as White, participants' hand movements nevertheless revealed a simultaneous attraction to select the other race-category response (stereotypically tied to the status cue) before arriving at a final categorization. Further, this attraction effect grew as race became more ambiguous (Experiment 2). Computational simulations then demonstrated that these effects may be accounted for by a neurally plausible person categorization system, in which contextual cues come to trigger stereotypes that in turn influence race perception. Together, the findings show how stereotypes interact with physical cues to shape person categorization, and suggest that social and contextual factors guide the perception of race.     

Kin recognition: evidence that humans can perceive both positive and negative relatedness

The evolution of spite entails actors imposing costs on 'negative' relatives: those who are less likely than chance to share the actor's alleles and therefore more likely to bear rival alleles. Yet, despite a considerable body of research confirming that organisms can recognize positive relatives, little research has shown that organisms can recognize negative relatives. Here, we extend previous work on human phenotype matching by introducing a cue to negative relatedness: negative self-resembling faces, which differ from an average face in the opposite direction to the way an individual's own face differs from the average. Participants made trustworthiness and attractiveness judgements of pairs of opposite-sex positive and negative self-resembling faces. Analyses revealed opposing effects of positive and negative self-resembling faces on trustworthiness and attractiveness judgements. This is the first clear evidence that humans are sensitive to negative relatedness cues, and suggests the potential for the adaptive allocation of spiteful behaviour.     

Short-term incidental memory for irrelevant cues

A new analysis of previously published studies of delayed matching-to-sample (DMTS) water-escape and the results of a new food-reinforced discrimination study are presented. In both cases, male Sprague-Dawley rats demonstrated short-term incidental memory for irrelevant cues in the context of two-alternative forced-choice problems that required learning about relevant cues. In the DMTS experiments, relevant and irrelevant cues were place or brightness. In the discrimination experiment, the relevant cues were place, brightness or a visual-tactile maze insert. In all experiments, after the rats attained high-level performance, consistently making choices with respect to the relevant stimuli, response latencies to the correct relevant cue were shorter when the irrelevant cue value(s) was the same as on the immediately preceding trial. These latency differences are interpreted as indicating that the rats demonstrated short-term incidental memory for the irrelevant cues. This mnemonic phenomenon resembles priming, an implicit form of memory.     

Action evaluation is modulated dominantly by internal sensorimotor information and partly by noncausal external cue

Previous studies demonstrated that human motor actions are not always monitored by perceptual awareness and that implicit motor control plays a key role in performing actions. In addition, appropriate evaluation of our own motor behavior is vital for human life. Here we combined a reaching task with a visual backward masking paradigm to induce an implicit motor response that is congruent or incongruent with the visual perception. We used this to investigate (i) how we evaluate such implicit motor response that could be inconsistent with perceptual awareness and (ii) the possible contributions of reaching error, external visual cues, and internal sensorimotor information to this evaluation. Participants were instructed, after each trial, to rate their own reaching performance on a 5-point scale (i.e., smooth-clumsy). They also needed to identify a color presented at a fixation point that could be changed just after the reaching start. The color was linked to the prime-mask congruency (i.e., congruent-green, incongruent-blue) in the practice phase, and then inconsistent pairs (congruent-blue or incongruent-green) were introduced in the test phase. We found early trajectory deviations induced by the invisible prime stimulus, and such implicit motor responses are significantly correlated with the action evaluation score. The results suggest the "conscious" action evaluation is properly monitoring online sensory outcomes derived by implicit motor control. Furthermore, statistical path analyses showed that internal sensorimotor information from the motor behavior modulated by the invisible prime was the predominant cue for the action evaluation, while the color-cue association learned in the practice phase in some cases biases the action evaluation in the test phase.     

Further Evidence against a Momentum Explanation for IOR

Reaction times to targets presented in the same location as a preceding cue are greater than those to targets presented opposite the cued location. This observation can be explained as a result of inhibition at the attended location (IOR), or as facilitation at the location opposite the cue (opposite facilitation effect or OFE). Past research has demonstrated that IOR is observed reliably, whereas OFE is observed only occasionally. The present series of four experiments allows us to determine whether or not OFE can be explained by eye movements as suggested by previous authors. Participants'' eye movements were monitored as they were presented with an array of four placeholders aligned with the four cardinal axes. Exogenous cues and targets were presented successively. Participants (N=37) completed either: i.) cue-manual and cue-saccade experiments, ignoring the cue and then responding with a keypress or saccade, respectively, or ii.) manual-manual and saccade-saccade experiments, responding to both the cue and the target with a keypress or saccade respectively. Results demonstrated a reliable IOR effect in each of the four experiments (reaction time greater for same versus adjacent and opposite cue-target trials). None of the four experiments demonstrated evidence of an OFE (reaction times were not significantly lower for opposite versus adjacent cue-target trials). These results are inconsistent with a momentum-based account of cue-target task performance, and furthermore suggest that the OFE cannot be attributed to occasional eye movements to the cue and/or target in previous studies.     

Neural Substrate of Initiation of Cross-Modal Working Memory Retrieval

Cross-modal working memory requires integrating stimuli from different modalities and it is associated with co-activation of distributed networks in the brain. However, how brain initiates cross-modal working memory retrieval remains not clear yet. In the present study, we developed a cued matching task, in which the necessity for cross-modal/unimodal memory retrieval and its initiation time were controlled by a task cue appeared in the delay period. Using functional magnetic resonance imaging (fMRI), significantly larger brain activations were observed in the left lateral prefrontal cortex (l-LPFC), left superior parietal lobe (l-SPL), and thalamus in the cued cross-modal matching trials (CCMT) compared to those in the cued unimodal matching trials (CUMT). However, no significant differences in the brain activations prior to task cue were observed for sensory stimulation in the l-LPFC and l-SPL areas. Although thalamus displayed differential responses to the sensory stimulation between two conditions, the differential responses were not the same with responses to the task cues. These results revealed that the frontoparietal-thalamus network participated in the initiation of cross-modal working memory retrieval. Secondly, the l-SPL and thalamus showed differential activations between maintenance and working memory retrieval, which might be associated with the enhanced demand for cognitive resources.     

Cues Used for Localizing Food by the Gray Squirrel (Sciurus carolinensis)

We compared the use of olfactory, visual, and spatial cues for learning the location of stored food by gray squirrels (Sciurus carolinensis). All experimental cues were extrinsic, that is, they originated from the environment around the food rather than from the food itself. In training trials, artificial caches with one of two odors, one of two colors, and six of 12 spatial locations contained sunflower seeds. In experimental trials, the odors, colors, and sets of spatial locations associated with food were reversed one at a time, so that only two of the three training cues gave evidence of the food rewards. Consequent declines in food localization by the squirrels revealed differential use of particular cue modalities. The data show that squirrels used visual cues the most and olfactory cues the least with this design. These results, along with other evidence, suggest that gray squirrels use spatial memory in food recovery.     

Hippocampus Is Place of Interaction between Unconscious and Conscious Memories

Recent evidence suggests that humans can form and later retrieve new semantic relations unconsciously by way of hippocampus—the key structure also recruited for conscious relational (episodic) memory. If the hippocampus subserves both conscious and unconscious relational encoding/retrieval, one would expect the hippocampus to be place of unconscious-conscious interactions during memory retrieval. We tested this hypothesis in an fMRI experiment probing the interaction between the unconscious and conscious retrieval of face-associated information. For the establishment of unconscious relational memories, we presented subliminal (masked) combinations of unfamiliar faces and written occupations (“actor” or “politician”). At test, we presented the former subliminal faces, but now supraliminally, as cues for the reactivation of the unconsciously associated occupations. We hypothesized that unconscious reactivation of the associated occupation—actor or politician—would facilitate or inhibit the subsequent conscious retrieval of a celebrity’s occupation, which was also actor or politician. Depending on whether the reactivated unconscious occupation was congruent or incongruent to the celebrity’s occupation, we expected either quicker or delayed conscious retrieval process. Conscious retrieval was quicker in the congruent relative to a neutral baseline condition but not delayed in the incongruent condition. fMRI data collected during subliminal face-occupation encoding confirmed previous evidence that the hippocampus was interacting with neocortical storage sites of semantic knowledge to support relational encoding. fMRI data collected at test revealed that the facilitated conscious retrieval was paralleled by deactivations in the hippocampus and neocortical storage sites of semantic knowledge. We assume that the unconscious reactivation has pre-activated overlapping relational representations in the hippocampus reducing the neural effort for conscious retrieval. This finding supports the notion of synergistic interactions between conscious and unconscious relational memories in a common, cohesive hippocampal-neocortical memory space.     

Eye-Catching Odors: Olfaction Elicits Sustained Gazing to Faces and Eyes in 4-Month-Old Infants

This study investigated whether an odor can affect infants'' attention to visually presented objects and whether it can selectively direct visual gaze at visual targets as a function of their meaning. Four-month-old infants (n = 48) were exposed to their mother''s body odors while their visual exploration was recorded with an eye-movement tracking system. Two groups of infants, who were assigned to either an odor condition or a control condition, looked at a scene composed of still pictures of faces and cars. As expected, infants looked longer at the faces than at the cars but this spontaneous preference for faces was significantly enhanced in presence of the odor. As expected also, when looking at the face, the infants looked longer at the eyes than at any other facial regions, but, again, they looked at the eyes significantly longer in the presence of the odor. Thus, 4-month-old infants are sensitive to the contextual effects of odors while looking at faces. This suggests that early social attention to faces is mediated by visual as well as non-visual cues.     

Social transmission of novel foraging behavior in bats: frog calls and their referents

The fringe-lipped bat, Trachops cirrhosus, uses prey-emitted acoustic cues (frog calls) to assess prey palatability . Previous experiments show that wild T. cirrhosus brought into the laboratory are flexible in their ability to reverse the associations they form between prey cues and prey quality . Here we asked how this flexibility can be achieved in nature. We quantified the rate at which bats learned to associate the calls of a poisonous toad species with palatable prey by placing bats in three groups: (a) social learning, in which a bat inexperienced with the novel association was allowed to observe an experienced bat; (b) social facilitation, in which two inexperienced bats were presented with the experimental task together; and (c) trial-and-error, in which a single inexperienced bat was presented with the experimental task alone. In the social-learning group, bats rapidly acquired the novel association in an average of 5.3 trials. In the social-facilitation and trial-and-error groups, most bats did not approach the call of the poisonous species after 100 trials. Thus, once acquired, novel associations between prey cue and prey quality could spread rapidly through the bat population by cultural transmission. This is the first case to document predator social learning of an acoustic prey cue.     

Cues used by male and female hooded rats for locating a brightness change

Entries of and time spent in a novel Y-maze arm that had changed from white (during acquisition trials) to black (during retention trials) were investigated in male and female Long-Evans hooded rats after the apparatus had been horizontally rotated through 180 degrees or left undisturbed. Maze rotation reduced responsiveness to this arm in males but not in females. When each arm was associated with a different set of visual cues, males significantly chose the novel arm only in the presence of intra- and extra-maze cues either alone or in combination. Females significantly selected the novel arm only in the absence of either type of cue, and in the presence of intra-maze cues alone. However, when the duration of acquisition trials was increased from 6 to 12min, females also selected the novel arm in the presence of both intra- and extra-maze cues. It was concluded that, while female rats appeared able to use egocentric (or response-related) cues for locating the novel arm, males were more dependent on allocentric (or place-related) cues following shorter acquisition trials. Because of the importance of such cues, it seemed that the task of recognizing which maze arm had changed in brightness defined the test as one of spatial memory.