Visuospatial Sequence Learning without Seeing

Background

The ability to detect and integrate associations between unrelated items that are close in space and time is a key feature of human learning and memory. Learning sequential associations between non-adjacent visual stimuli (higher-order visuospatial dependencies) can occur either with or without awareness (explicit vs. implicit learning) of the products of learning. Existing behavioural and neurocognitive studies of explicit and implicit sequence learning, however, are based on conscious access to the sequence of target locations and, typically, on conditions where the locations for orienting, or motor, responses coincide with the locations of the target sequence.

Methodology/Principal Findings

Dichoptic stimuli were presented on a novel sequence learning task using a mirror stereoscope to mask the eye-of-origin of visual input from conscious awareness. We demonstrate that conscious access to the sequence of target locations and responses that coincide with structure of the target sequence are dispensable features when learning higher-order visuospatial associations. Sequence knowledge was expressed in the ability of participants to identify the trained higher-order visuospatial sequence on a recognition test, even though the trained and untrained recognition sequences were identical when viewed at a conscious binocular level, and differed only at the level of the masked sequential associations.

Conclusions/Significance

These results demonstrate that unconscious processing can support perceptual learning of higher-order sequential associations through interocular integration of retinotopic-based codes stemming from monocular eye-of-origin information. Furthermore, unlike other forms of perceptual associative learning, visuospatial attention did not need to be directed to the locations of the target sequence. More generally, the results pose a challenge to neural models of learning to account for a previously unknown capacity of the human visual system to support the detection, learning and recognition of higher-order sequential associations under conditions where observers are unable to see the target sequence or perform responses that coincide with structure of the target sequence.     

Does Consolidation of Visuospatial Sequence Knowledge Depend on Eye Movements?

In the current study, we assessed whether visuospatial sequence knowledge is retained over 24 hours and whether this retention is dependent on the occurrence of eye movements. Participants performed two sessions of a serial reaction time (SRT) task in which they had to manually react to the identity of a target letter pair presented in one of four locations around a fixation cross. When the letter pair ‘XO’ was presented, a left response had to be given, when the letter pair ‘OX’ was presented, a right response was required. In the Eye Movements (EM) condition, eye movements were necessary to perform the task since the fixation cross and the target were separated by at least 9° visual angle. In the No Eye Movements (NEM) condition, on the other hand, eye movements were minimized by keeping the distance from the fixation cross to the target below 1° visual angle and by limiting the stimulus presentation to 100 ms. Since the target identity changed randomly in both conditions, no manual response sequence was present in the task. However, target location was structured according to a deterministic sequence in both the EM and NEM condition. Learning of the target location sequence was determined at the end of the first session and 24 hours after initial learning. Results indicated that the sequence learning effect in the SRT task diminished, yet remained significant, over the 24 hour interval in both conditions. Importantly, the difference in eye movements had no impact on the transfer of sequence knowledge. These results suggest that the retention of visuospatial sequence knowledge occurs alike, irrespective of whether this knowledge is supported by eye movements or not.     

Asymmetrical generalisation between pheromonal and floral odours in appetitive olfactory conditioning of the honey bee (Apis mellifera L.)

The capacity to generalise between similar but not identical olfactory stimuli is crucial for honey bees, allowing them to find rewarding food sources with varying volatile emissions. We studied bees' generalisation behaviour with odours having different biological values: typical floral odours or alarm compounds. Bees' behavioural and peripheral electrophysiological responses were investigated using a combined proboscis extension response conditioning-electroantennogram assay. Bees were conditioned to pure linalool (floral) or to pure isoamyl acetate (alarm) and were tested with different concentrations of both compounds. Electrophysiological responses were not influenced by conditioning, suggesting that the learning of individual compounds does not rely on modulations of peripheral sensitivity. Behaviourally, generalisation responses of bees conditioned to the alarm compound were much higher than those of bees conditioned to the floral odour. We further demonstrated such asymmetrical generalisation between alarm and floral odours by using differential conditioning procedures. Conditioning to alarm compounds (isoamyl acetate or 2-heptanone) consistently induced more generalisation than conditioning to floral compounds (linalool or phenylacetaldehyde). Interestingly, generalisation between the two alarm compounds, which are otherwise chemically different, was extremely high. These results are discussed in relation to the neural representation of compounds with different biological significance for bees.     

Effects of the pharmacologic manipulation of testosterone on cognitive functioning in women with polycystic ovary syndrome: a randomized, placebo-controlled treatment study

In a previous study, we found that women with polycystic ovary syndrome (PCOS), an endocrine disorder characterized by chronic hyperandrogenism, performed more poorly than healthy, matched controls on a number of neuropsychological tests, in particular tests of verbal fluency, verbal memory, manual dexterity, and visuospatial working memory. This randomized, placebo-controlled trial was undertaken to investigate whether pharmacologic manipulation of free testosterone (free T) levels in women with PCOS might affect their performance on cognitive tests. Nineteen women with PCOS completed a battery of neuropsychological tests before and after 3 months of treatment with either an anti-androgen (cyproterone acetate) plus estrogen or with a placebo. Hormone treatment of women with PCOS caused a significant reduction in their free T levels but did not affect performance on tests visuospatial ability, verbal memory, manual dexterity, or perceptual speed. Women treated with hormone therapy did, however, demonstrate an improvement in their performance on a test of verbal fluency compared to their pre-treatment scores. These findings suggest that changes in free T levels do not have a significant impact on cognitive performance in women with PCOS, although reductions in free T may be beneficial for verbal fluency.     

Effect of Exogenous Cues on Covert Spatial Orienting in Deaf and Normal Hearing Individuals

Deaf individuals have been known to process visual stimuli better at the periphery compared to the normal hearing population. However, very few studies have examined attention orienting in the oculomotor domain in the deaf, particularly when targets appear at variable eccentricity. In this study, we examined if the visual perceptual processing advantage reported in the deaf people also modulates spatial attentional orienting with eye movement responses. We used a spatial cueing task with cued and uncued targets that appeared at two different eccentricities and explored attentional facilitation and inhibition. We elicited both a saccadic and a manual response. The deaf showed a higher cueing effect for the ocular responses than the normal hearing participants. However, there was no group difference for the manual responses. There was also higher facilitation at the periphery for both saccadic and manual responses, irrespective of groups. These results suggest that, owing to their superior visual processing ability, the deaf may orient attention faster to targets. We discuss the results in terms of previous studies on cueing and attentional orienting in deaf.     

Robot Guided ‘Pen Skill’ Training in Children with Motor Difficulties

Motor deficits are linked to a range of negative physical, social and academic consequences. Haptic robotic interventions, based on the principles of sensorimotor learning, have been shown previously to help children with motor problems learn new movements. We therefore examined whether the training benefits of a robotic system would generalise to a standardised test of ‘pen-skills’, assessed using objective kinematic measures [via the Clinical Kinematic Assessment Tool, CKAT]. A counterbalanced, cross-over design was used in a group of 51 children (37 male, aged 5–11 years) with manual control difficulties. Improved performance on a novel task using the robotic device could be attributed to the intervention but there was no evidence of generalisation to any of the CKAT tasks. The robotic system appears to have the potential to support motor learning, with the technology affording numerous advantages. However, the training regime may need to target particular manual skills (e.g. letter formation) in order to obtain clinically significant improvements in specific skills such as handwriting.     

The Neural Correlates of Visuospatial Perceptual and Oculomotor Extrapolation

The human visual system must perform complex visuospatial extrapolations (VSE) across space and time in order to extract shape and form from the retinal projection of a cluttered visual environment characterized by occluded surfaces and moving objects. Even if we exclude the temporal dimension, for instance when judging whether an extended finger is pointing towards one object or another, the mechanisms of VSE remain opaque. Here we investigated the neural correlates of VSE using functional magnetic resonance imaging in sixteen human observers while they judged the relative position of, or saccaded to, a (virtual) target defined by the extrapolated path of a pointer. Using whole brain and region of interest (ROI) analyses, we compared the brain activity evoked by these VSE tasks to similar control judgements or eye movements made to explicit (dot) targets that did not require extrapolation. The data show that activity in an occipitotemporal region that included the lateral occipital cortex (LOC) was significantly greater during VSE than during control tasks. A similar, though less pronounced, pattern was also evident in regions of the fronto-parietal cortex that included the frontal eye fields. However, none of the ROIs examined exhibited a significant interaction between target type (extrapolated/explicit) and response type (oculomotor/perceptual). These findings are consistent with a close association between visuoperceptual and oculomotor responses, and highlight a critical role for the LOC in the process of VSE.     

Dissociation between the Espinet and perceptual learning effects in flavour aversion conditioning

In three experiments rats were given pre-exposure to two compound flavours, AX and BX, the two compounds being presented for some subjects on alternate trials (the intermixed schedule) and, for others, in separate blocks of trials (the blocked schedule). After aversion conditioning with A (in Experiments 1 and 2), the inhibitory properties of B were tested using both retardation (Experiment 1) and summation tests (Experiment 2). The results failed to support the proposal [Anim. Learn. Behav. 23 (1995) 361] that B should acquire inhibitory properties in the intermixed condition (the "Espinet effect"). Experiment 3 demonstrated that generalisation to BX after conditioning with AX was attenuated by intermixed pre-exposure (a perceptual learning effect). This pattern of results challenges the hypothesis that inhibitory learning during intermixed pre-exposure to AX and BX can account for both the Espinet and the perceptual learning effects.     

Field but not lab paradigms support generalisation by predators of aposematic polymorphic prey: the Oophaga histrionica complex

The persistence of novel aposematic forms, and thereby the evolution of aposematic polymorphism, remain intriguing. Novel and rare forms could be disproportionally attacked by predators that already learned to avoid a pre-existing and more common aposematic form. Alternatively, novel forms could be less frequently attacked if predators are reluctant to attack unknown potential prey (neophobia) or if previous learning allows them to generalise and recognise the novel form as toxic. We used colour variation in polymorphic poison frogs (Oophaga histrionica complex) to test whether predators familiar with one aposematic form do generalise their avoidance behaviour to other aposematic forms. To strengthen our inference, we combined a field test of attack rates to local and non-local models with a lab experiment of generalisation capabilities by newly born chicks. Field predators attacked a significantly lower proportion of 529 aposematic compared to 150 cryptic models. Predators co-occurring with the local aposematic form of O. histrionica equally avoided non-local forms, especially in areas where the species was abundant. Forty-two lab chicks learned to discriminate between an aposematic and a cryptic image, but failed to generalise to other aposematic images, even though we tried with six combinations of aposematic forms. To better mimic the situation in the field, we further tested whether chicks trained with a set of four simultaneous aposematic images would generalise better. They failed to learn the discrimination task. Our data contrast with previous field studies on other poison frogs, and support a role for generalisation, and arguably not neophobia, in predator avoidance of novel aposematic forms.     

Can We Improve Structured Sequence Processing? Exploring the Direct and Indirect Effects of Computerized Training Using a Mediational Model

Recent research suggests that language acquisition may rely on domain-general learning abilities, such as structured sequence processing, which is the ability to extract, encode, and represent structured patterns in a temporal sequence. If structured sequence processing supports language, then it may be possible to improve language function by enhancing this foundational learning ability. The goal of the present study was to use a novel computerized training task as a means to better understand the relationship between structured sequence processing and language function. Participants first were assessed on pre-training tasks to provide baseline behavioral measures of structured sequence processing and language abilities. Participants were then quasi-randomly assigned to either a treatment group involving adaptive structured visuospatial sequence training, a treatment group involving adaptive non-structured visuospatial sequence training, or a control group. Following four days of sequence training, all participants were assessed with the same pre-training measures. Overall comparison of the post-training means revealed no group differences. However, in order to examine the potential relations between sequence training, structured sequence processing, and language ability, we used a mediation analysis that showed two competing effects. In the indirect effect, adaptive sequence training with structural regularities had a positive impact on structured sequence processing performance, which in turn had a positive impact on language processing. This finding not only identifies a potential novel intervention to treat language impairments but also may be the first demonstration that structured sequence processing can be improved and that this, in turn, has an impact on language processing. However, in the direct effect, adaptive sequence training with structural regularities had a direct negative impact on language processing. This unexpected finding suggests that adaptive training with structural regularities might potentially interfere with language processing. Taken together, these findings underscore the importance of pursuing designs that promote a better understanding of the mechanisms underlying training-related changes, so that regimens can be developed that help reduce these types of negative effects while simultaneously maximizing the benefits to outcome measures of interest.     

Perceptual and neural olfactory similarity in honeybees

The question of whether or not neural activity patterns recorded in the olfactory centres of the brain correspond to olfactory perceptual measures remains unanswered. To address this question, we studied olfaction in honeybees Apis mellifera using the olfactory conditioning of the proboscis extension response. We conditioned bees to odours and tested generalisation responses to different odours. Sixteen odours were used, which varied both in their functional group (primary and secondary alcohols, aldehydes and ketones) and in their carbon-chain length (from six to nine carbons).The results obtained by presentation of a total of 16 × 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between long-chain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity. We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours.     

Ego Depletion Impairs Implicit Learning

Implicit skill learning occurs incidentally and without conscious awareness of what is learned. However, the rate and effectiveness of learning may still be affected by decreased availability of central processing resources. Dual-task experiments have generally found impairments in implicit learning, however, these studies have also shown that certain characteristics of the secondary task (e.g., timing) can complicate the interpretation of these results. To avoid this problem, the current experiments used a novel method to impose resource constraints prior to engaging in skill learning. Ego depletion theory states that humans possess a limited store of cognitive resources that, when depleted, results in deficits in self-regulation and cognitive control. In a first experiment, we used a standard ego depletion manipulation prior to performance of the Serial Interception Sequence Learning (SISL) task. Depleted participants exhibited poorer test performance than did non-depleted controls, indicating that reducing available executive resources may adversely affect implicit sequence learning, expression of sequence knowledge, or both. In a second experiment, depletion was administered either prior to or after training. Participants who reported higher levels of depletion before or after training again showed less sequence-specific knowledge on the post-training assessment. However, the results did not allow for clear separation of ego depletion effects on learning versus subsequent sequence-specific performance. These results indicate that performance on an implicitly learned sequence can be impaired by a reduction in executive resources, in spite of learning taking place outside of awareness and without conscious intent.     

Testosterone levels and cognitive functioning in women with polycystic ovary syndrome and in healthy young women

We investigated the possible influence of testosterone (T) on cognitive functioning in women with polycystic ovary syndrome (PCOS), an endocrine disorder associated with elevated levels of free testosterone (free T). Performance on a battery of neuropsychological tests in 29 women with elevated free T levels due to PCOS was compared to the performance of 22 age- and education-matched, healthy control women with free T levels in the normal female range. Women with PCOS had significantly higher levels of free T (estimated by the free androgen index) and demonstrated significantly worse performance on tests of verbal fluency, verbal memory, manual dexterity, and visuospatial working memory than the healthy control women. No differences between the groups were found on tests of mental rotation, spatial visualization, spatial perception, or perceptual speed. These results suggest that, in women, elevations in free T may be associated with poorer performance on cognitive tasks that tend to show a female advantage.     

Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices

It is widely presumed that odor quality is a direct outcome of odorant structure, but human studies indicate that molecular knowledge of an odorant is not always sufficient to predict odor quality. Indeed, the same olfactory input may generate different odor percepts depending on prior learning and experience. Combining functional magnetic resonance imaging with an olfactory paradigm of perceptual learning, we examined how sensory experience modifies odor perception and odor quality coding in the human brain. Prolonged exposure to a target odorant enhanced perceptual differentiation for odorants related in odor quality or functional group, an effect that was paralleled by learning-induced response increases in piriform cortex and orbitofrontal cortex (OFC). Critically, the magnitude of OFC activation predicted subsequent improvement in behavioral differentiation. Our findings suggest that neural representations of odor quality can be rapidly updated through mere perceptual experience, a mechanism that may underlie the development of odor perception.     

Female mini-pig performance of temporal response differentiation, incremental repeated acquisition, and progressive ratio operant tasks

Increased knowledge of the cognitive abilities of mini-pigs is needed due to their increasing use in behavioral neuroscience research. Here, six female Yucatan mini-pigs performed tasks thought to measure timing behavior (temporal response differentiation, TRD), learning (incremental repeated acquisition, IRA), and motivation (progressive ratio, PR). Daily 30-min sessions for food reinforcers required a lever press be maintained for at least 10 but no longer than 14s (TRD), learning a new sequence of lever presses each test day (IRA) or an escalating number of presses for subsequent reinforcers (PR). All animals performed PR two days/week while three performed TRD five days/week and the other three performed IRA five days/week. Over the four test weeks, no animal completed TRD training and only one appeared to progress. For this task, lever press maintenance appeared difficult since by choice, the pigs used a front hoof, rather than the snout, to press the lever. IRA subjects showed gradually increasing performance with response rates comparable to those of rats but below those of children and monkeys and accuracy below that for rats. PR response rates were higher than those typically reported for rats, but lower than for adult rhesus monkeys or children. Physical differences in the way that each species responds likely account for these differences.     

Changes in stimulus control during guided skill learning in rats

We examined the changes in stimulus control occurring during guided skill learning in rats. Twenty rats were trained to complete a left-right sequence of lever presses guided by the onset and offset of panel lights over their respective levers. Once sequence accuracy was high and stable, the rats were divided into two groups. For the No-Lights group, the lights were eliminated without changing the response requirements. Sequence accuracy decreased in all subjects, but accuracy was higher than that predicted by random chance. More practice produced greater autonomy and reduced dependence on the guiding lights. For the Reversed-Lights group, the lights were presented in reversed order without changing the response requirements. Sequence accuracy immediately plummeted and did not recover, violating expectations of automatization. The guiding lights appeared to overshadow other sources of stimulus control.     

Visuospatial Attention to Single and Multiple Objects Is Independently Impaired in Parkinson's Disease

Parkinson’s disease (PD) is associated with deficits in visuospatial attention. It is as yet unknown whether these attentional deficits begin at a perceptual level or instead reflect disruptions in oculomotor or higher-order processes. In the present study, non-demented individuals with PD and matched normal control adults (NC) participated in two tasks requiring sustained visuospatial attention, both based on a multiple object tracking paradigm. Eye tracking was used to ensure central fixation. In Experiment 1 (26 PD, 21 NC), a pair of identical red dots (one target, one distractor) rotated randomly for three seconds at varied speeds. The task was to maintain the identity of the sole target, which was labeled prior to each trial. PD were less accurate than NC overall (p = .049). When considering only trials where fixation was maintained, however, there was no significant group difference, suggesting that the deficit’s origin is closely related to oculomotor processing. To determine whether PD had additional impairment in multifocal attention, in Experiment 2 (25 PD, 15 NC), two targets were presented along with distractors at a moderate speed, along with a control condition in which dots remained stationary. PD were less accurate than NC for moving (p = 0.02) but not stationary targets. This group difference remained significant when considering only trials where fixation was maintained, suggesting the source of the PD deficit was independent from oculomotor processing. Taken together, the results implicate separate mechanisms for single vs. multiple object tracking deficits in PD.     

Imaging emotional brain functions: Conceptual and methodological issues

This article reviews the psychophysiological and brain imaging literature on emotional brain function from a methodological point of view. The difficulties in defining, operationalising and measuring emotional activation and, in particular, aversive learning will be considered. Emotion is a response of the organism during an episode of major significance and involves physiological activation, motivational, perceptual, evaluative and learning processes, motor expression, action tendencies and monitoring/subjective feelings. Despite the advances in assessing the physiological correlates of emotional perception and learning processes, a critical appraisal shows that functional neuroimaging approaches encounter methodological difficulties regarding measurement precision (e.g., response scaling and reproducibility) and validity (e.g., response specificity, generalisation to other paradigms, subjects or settings). Since emotional processes are not only the result of localised but also of widely distributed activation, a more representative model of assessment is needed that systematically relates the hierarchy of high- and low-level emotion constructs with the corresponding patterns of activity and functional connectivity of the brain.     

Eye position affects orienting of visuospatial attention

The ability to detect an incoming visual stimulus is enhanced by knowledge of stimulus location (orienting of visuospatial attention). Although the brain mechanisms at the basis of this enhancement are not yet fully clarified, there is evidence that orienting of attention is accompanied by the activation of oculomotor circuits. It remains unclear, however, whether this oculomotor activity is an epiphenomenon or is functionally related to the attentional process. Attentional benefits are usually measured by the classical Posner paradigm. When subjects fixate centrally and are requested to detect a visual stimulus that could appear in an attended or unattended location, they react faster to stimuli appearing in the attended one. Here, we demonstrate that in monocular vision visuospatial attention was significantly modulated by the position of the eye in the orbit. When the screen was placed 40 degrees to the right or to the left of subjects' sagittal plane, attentional benefits for stimuli appearing in subjects' temporal spatial hemifield dramatically decayed, even if the retinal stimulation was exactly the same as in the classical paradigm. The finding that eyes and attention show a common limit stop point supports their close functional coupling.     

The control of gaze (2): cortical control of ocular saccades: functional brain imaging data

Saccades are very rapid eye movements allowing us to explore the visual world. Although most of the time unconscious, the programming of each saccade implies a complex decision which depends upon both the perceptual context and the intentions of the subject. The cerebral cortex is critically involved in deciding where, when and in which sequence we move the eyes. Using sophisticated experimental designs, such as the learning of sequences of saccades, has revealed that besides a core fronto-parietal circuit, prefrontal, cingulate, and mediotemporal regions seem critically involved in higher level oculomotor control. Understanding precisely the cortical networks associated to different components of ocular movements can certainly be very useful to characterize, test, and eventually detect various kinds of neurological pathology.