Hemispheric Asymmetries in Repetition Enhancement and Suppression Effects in the Newborn Brain

Background

The repeated presentation of stimuli typically attenuates neural responses (repetition suppression) or, less commonly, increases them (repetition enhancement) when stimuli are highly complex, degraded or presented under noisy conditions. In adult functional neuroimaging research, these repetition effects are considered as neural correlates of habituation. The development and respective functional significance of these effects in infancy remain largely unknown.

Objective

This study investigates repetition effects in newborns using functional near-infrared spectroscopy, and specifically the role of stimulus complexity in evoking a repetition enhancement vs. a repetition suppression response, following up on Gervain et al. (2008). In that study, abstract rule-learning was found at birth in cortical areas specific to speech processing, as evidenced by a left-lateralized repetition enhancement of the hemodynamic response to highly variable speech sequences conforming to a repetition-based ABB artificial grammar, but not to a random ABC grammar.

Methods

Here, the same paradigm was used to investigate how simpler stimuli (12 different sequences per condition as opposed to 140), and simpler presentation conditions (blocked rather than interleaved) would influence repetition effects at birth.

Results

Results revealed that the two grammars elicited different dynamics in the two hemispheres. In left fronto-temporal areas, we reproduce the early perceptual discrimination of the two grammars, with ABB giving rise to a greater response at the beginning of the experiment than ABC. In addition, the ABC grammar evoked a repetition enhancement effect over time, whereas a stable response was found for the ABB grammar. Right fronto-temporal areas showed neither initial discrimination, nor change over time to either pattern.

Conclusion

Taken together with Gervain et al. (2008), this is the first evidence that manipulating methodological factors influences the presence or absence of neural repetition enhancement effects in newborns and stimulus variability appears a particularly important factor. Further, this temporal modulation is restricted to the left hemisphere, confirming its specialization for learning linguistic regularities from birth.     

Neuroimaging evidence for processes underlying repetition of ignored stimuli

Prolonged response times are observed with targets having been presented as distractors immediately before, called negative priming effect. Among others, inhibitory and retrieval processes have been suggested underlying this behavioral effect. As those processes would involve different neural activation patterns, a functional magnetic resonance imaging (fMRI) study including 28 subjects was conducted. Two tasks were used to investigate stimulus repetition effects. One task focused on target location, the other on target identity. Both tasks are known to elicit the expected response time effects. However, there is less agreement about the relationship of those tasks with the explanatory accounts under consideration. Based on within-subject comparisons we found clear differences between the experimental repetition conditions and the neutral control condition on neural level for both tasks. Hemodynamic fronto-striatal activation patterns occurred for the location-based task favoring the selective inhibition account. Hippocampal activation found for the identity-based task suggests an assignment to the retrieval account; however, this task lacked a behavioral effect.     

Automatic Imitation in Rhythmical Actions: Kinematic Fidelity and the Effects of Compatibility,Delay, and Visual Monitoring

We demonstrate that observation of everyday rhythmical actions biases subsequent motor execution of the same and of different actions, using a paradigm where the observed actions were irrelevant for action execution. The cycle time of the distractor actions was subtly manipulated across trials, and the cycle time of motor responses served as the main dependent measure. Although distractor frequencies reliably biased response cycle times, this imitation bias was only a small fraction of the modulations in distractor speed, as well as of the modulations produced when participants intentionally imitated the observed rhythms. Importantly, this bias was not only present for compatible actions, but was also found, though numerically reduced, when distractor and executed actions were different (e.g., tooth brushing vs. window wiping), or when the dominant plane of movement was different (horizontal vs. vertical). In addition, these effects were equally pronounced for execution at 0, 4, and 8 s after action observation, a finding that contrasts with the more short-lived effects reported in earlier studies. The imitation bias was also unaffected when vision of the hand was occluded during execution, indicating that this effect most likely resulted from visuomotor interactions during distractor observation, rather than from visual monitoring and guidance during execution. Finally, when the distractor was incompatible in both dimensions (action type and plane) the imitation bias was not reduced further, in an additive way, relative to the single-incompatible conditions. This points to a mechanism whereby the observed action’s impact on motor processing is generally reduced whenever this is not useful for motor planning. We interpret these findings in the framework of biased competition, where intended and distractor actions can be represented as competing and quasi-encapsulated sensorimotor streams.     

The effect of study-test modalities on the remembrance of subjective duration from long-term memory

It was examined whether stimulus modality (auditory vs. visual) affects the retrieval of subjective duration from memory. In two experiments the temporal generalization paradigm was used. Participants had to decide whether the previously learned standard duration (400 ms) occurred in the context of comparison stimuli. Two major results were found. (1) Discrimination was more accurate if the training and testing stimuli were of the same modality than if they were of opposite modalities. (2) If both modality of learning and modality of testing were different, subjects systematically underestimated the test durations, i.e. temporal generalization gradients (the proportion of identifications of a stimulus as the standard, plotted against stimulus duration) shifted to the right. The observed shift is interpreted as a result of a delayed timing process.     

Dissociation of category versus item priming in face processing: an event-related potential study

The underlying specificity of visual object categorization and discrimination can be elucidated by studying different types of repetition priming. Here we focused on this issue in face processing. We investigated category priming (i.e. the prime and target stimuli represent different exemplars of the same object category) and item priming (i.e. the prime and target stimuli are exactly the same image), using an immediate repetition paradigm. Twenty-three subjects were asked to respond as fast and accurately as possible to categorize whether the target stimulus was a face or a building image, but to ignore the prime stimulus. We recorded event-related potentials (ERPs) and reaction times (RTs) simultaneously. The RT data showed significant effects of category priming in both face trials and building trials, as well as a significant effect of item priming in face trials. With respect to the ERPs, in face trials, no priming effect was observed at the P100 stage, whereas a category priming effect emerged at the N170 stage, and an item priming effect at the P200 stage. In contrast, in building trials, priming effects occurred already at the P100 stage. Our results indicated that distinct neural mechanisms underlie separable kinds of immediate repetition priming in face processing.     

Photoresponse and Learning Behavior of Ascidian Larvae, a Primitive Chordate, to Repeated Stimuli of Step-Up and Step-Down of Light

Ascidians are lower chordates and their simple tadpole-like larvae share a basic body plan with vertebrates. Newly hatched larvae show no response to a stimulus of light. 4 h after hatching, the larvae were induced to swim upon a step-down of light and stop swimming upon a step-up of light. At weaker intensity of light, the larvae show the same response to a stimulus after presentation of repeated stimuli. When intensity of actinic light was increased, the larvae show sensitization and habituation of the swimming response to a stimulus after repeated stimuli of step-down and step-up of the light. Between 2 h 20 min and 3 h 40 min after hatching the larvae did not show any response to the first stimulus, but after several repeatedstimuli they show swimming response to a step-down of light. A repeated series of stimulus cause sensitization. Between 4 h and 7 h after hatching, the larvae show photoresponse to the first stimulus, but after several repetition of the stimuli, the larvae could not stop swimming to a stimulus of a step-up of the actinic light. A repeated series of stimulus cause greaterhabituation. Both sensitization and habituation depend upon intensity ofactinic light.     

Startle Auditory Stimuli Enhance the Performance of Fast Dynamic Contractions

Fast reaction times and the ability to develop a high rate of force development (RFD) are crucial for sports performance. However, little is known regarding the relationship between these parameters. The aim of this study was to investigate the effects of auditory stimuli of different intensities on the performance of a concentric bench-press exercise. Concentric bench-presses were performed by thirteen trained subjects in response to three different conditions: a visual stimulus (VS); a visual stimulus accompanied by a non-startle auditory stimulus (AS); and a visual stimulus accompanied by a startle auditory stimulus (SS). Peak RFD, peak velocity, onset movement, movement duration and electromyography from pectoralis and tricep muscles were recorded. The SS condition induced an increase in the RFD and peak velocity and a reduction in the movement onset and duration, in comparison with the VS and AS condition. The onset activation of the pectoralis and tricep muscles was shorter for the SS than for the VS and AS conditions. These findings point out to specific enhancement effects of loud auditory stimulation on the rate of force development. This is of relevance since startle stimuli could be used to explore neural adaptations to resistance training.     

Content-specific working memory modulation of the attentional blink

Three experiments were conducted to investigate the effects of working memory content on temporal attention in a rapid serial visual presentation attentional blink paradigm. It was shown that categorical similarity between working memory content and the target stimuli pertaining to the attentional task (both digits) increased attentional blink magnitude compared to a condition in which this similarity was absent (colors and digits, respectively). This effect was only observed when the items in working memory were not presented as conjunctions of the involved categories (i.e., colored digits). This suggested that storage and retrieval from working memory was at least preferentially conjunctive in this case. It was furthermore shown that the content of working memory enhanced the identification rate of the second target, by means of repetition priming, when inter-target lag was short and the attentional blink was in effect. The results are incompatible with theories of temporal attention that assume working memory has no causal role in the attentional blink and support theories that do.     

Evidence Inhibition Responds Reactively to the Salience of Distracting Information during Focused Attention

Along with target amplification, distractor inhibition is regarded as a major contributor to selective attention. Some theories suggest that the strength of inhibitory processing is proportional to the salience of the distractor (i.e., inhibition reacts to the distractor intensity). Other theories suggest that the strength of inhibitory processing does not depend on the salience of the distractor (i.e., inhibition does not react to the distractor intensity). The present study aimed to elucidate the relationship between the intensity of a distractor and its subsequent inhibition during focused attention. A flanker task with a variable distractor-target stimulus-onset asynchrony (SOA) was used to measure both distractor interference and distractor inhibition. We manipulated the intensity of the distractor in two separate ways, by varying its distance from the target (Experiment 1) and by varying its brightness (Experiment 2). The results indicate that more intense distractors were associated with both increased interference and stronger distractor inhibition. The latter outcome provides novel support for the reactive inhibition hypothesis, which posits that inhibition reacts to the strength of distractor input, such that more salient distractors elicit stronger inhibition.     

Selectivity of visual cortical neurons of rabbits to magnitude of moving stimuli

Unit responses of the rabbit visual cortex were investigated in relation to size of visual stimuli moving in their receptive field. With an increase in size of the stimulus in a direction perpendicular to the direction of movement ("width" of the stimulus) an initial increase in the intensity of the unit response through spatial summation of excitory effects is followed by a decrease through lateral inhibition. This inhibition is observed between zones of the receptive field which behave as activating when tested by a stimulus of small size. Each neuron has its own "preferred" size of stimuli evoking its maximal activation. No direct correlation is found between the "preferred" stimulus size and the size of the receptive field. With a change in stimulus size in the direction of movement ("length" of the stimulus) the responses to stimuli of optimal size may be potentiated through mutual facilitation of the effects evoked by the leading and trailing edges of the stimulus and weakened in response to stimuli of large size. The selective behavior of the neurons with respect to stimulus size is intensified in the case of coordinated changes in their length and width. It is postulated that the series of neurons responding to stimuli of different "preferred" dimensions may constitute a system classifying stimuli by their size.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 4, No. 6, pp. 636–644, November–December, 1972.     

The Spatial Structure of Stimuli Shapes the Timescale of Correlations in Population Spiking Activity

Throughout the central nervous system, the timescale over which pairs of neural spike trains are correlated is shaped by stimulus structure and behavioral context. Such shaping is thought to underlie important changes in the neural code, but the neural circuitry responsible is largely unknown. In this study, we investigate a stimulus-induced shaping of pairwise spike train correlations in the electrosensory system of weakly electric fish. Simultaneous single unit recordings of principal electrosensory cells show that an increase in the spatial extent of stimuli increases correlations at short () timescales while simultaneously reducing correlations at long () timescales. A spiking network model of the first two stages of electrosensory processing replicates this correlation shaping, under the assumptions that spatially broad stimuli both saturate feedforward afferent input and recruit an open-loop inhibitory feedback pathway. Our model predictions are experimentally verified using both the natural heterogeneity of the electrosensory system and pharmacological blockade of descending feedback projections. For weak stimuli, linear response analysis of the spiking network shows that the reduction of long timescale correlation for spatially broad stimuli is similar to correlation cancellation mechanisms previously suggested to be operative in mammalian cortex. The mechanism for correlation shaping supports population-level filtering of irrelevant distractor stimuli, thereby enhancing the population response to relevant prey and conspecific communication inputs.     

Diffuse Optical Tomography Activation in the Somatosensory Cortex: Specific Activation by Painful vs. Non-Painful Thermal Stimuli

Background

Pain is difficult to assess due to the subjective nature of self-reporting. The lack of objective measures of pain has hampered the development of new treatments as well as the evaluation of current ones. Functional MRI studies of pain have begun to delineate potential brain response signatures that could be used as objective read-outs of pain. Using Diffuse Optical Tomography (DOT), we have shown in the past a distinct DOT signal over the somatosensory cortex to a noxious heat stimulus that could be distinguished from the signal elicited by innocuous mechanical stimuli. Here we further our findings by studying the response to thermal innocuous and noxious stimuli.

Methodology/Principal Findings

Innocuous and noxious thermal stimuli were applied to the skin of the face of the first division (ophthalmic) of the trigeminal nerve in healthy volunteers (N = 6). Stimuli temperatures were adjusted for each subject to evoke warm (equivalent to a 3/10) and painful hot (7/10) sensations in a verbal rating scale (0/10 = no/max pain). A set of 26 stimuli (5 sec each) was applied for each temperature with inter-stimulus intervals varied between 8 and 15 sec using a Peltier thermode. A DOT system was used to capture cortical responses on both sides of the head over the primary somatosensory cortical region (S1). For the innocuous stimuli, group results indicated mainly activation on the contralateral side with a weak ipsilateral response. For the noxious stimuli, bilateral activation was observed with comparable amplitudes on both sides. Furthermore, noxious stimuli produced a temporal biphasic response while innocuous stimuli produced a monophasic response.

Conclusions/Significance

These results are in accordance with fMRI and our other DOT studies of innocuous mechanical and noxious heat stimuli. The data indicate the differentiation of DOT cortical responses for pain vs. innocuous stimuli that may be useful in assessing objectively acute pain.     

<Emphasis Type="Italic">P</Emphasis>300-based brain-computer interface: The effect of the stimulus position in a stimulus train

The most popular type of brain-computer interfaces (BCIs) are based on the detection of the P300 wave of the evoked potentials appearing in response to a stimulus chosen by the subject. In order to increase the speed of operation of these BCIs, it is possible to decrease the number of repeated stimulus presentations. It is associated with an increase in the relative importance of the response to the first stimulus in a train for correct recognition of the stimulus chosen. Event-related potentials (ERPs) in response to the first stimulus presentations are known to have their own specificity. Particularly, in many cases, the amplitude of the response to the first presentations is enhanced, which makes it very suitable for recognition in a BCI. However, this effect has not been studied to date. In this study, the ERPs recorded in healthy subjects in a standard BCI paradigm (n = 14) with ten presentations of stimuli or during triple-trial (n = 6) and single-trial (n = 6) presentations of stimuli in a modified BCI paradigm with moving objects have been analyzed. In both cases, first presentations of the target stimuli or single-trial presentation of the target stimulus were associated with higher amplitudes of ERPs. The opportunity to use specific differences between the responses to the first or single-trial presentations and the responses to later stimuli during their repeated presentations for improving high-speed operations in the P300-based BCI is discussed.     

The Effects of Stimulus Variability on the Perceptual Learning of Speech and Non-Speech Stimuli

Previous studies suggest fundamental differences between the perceptual learning of speech and non-speech stimuli. One major difference is in the way variability in the training set affects learning and its generalization to untrained stimuli: training-set variability appears to facilitate speech learning, while slowing or altogether extinguishing non-speech auditory learning. We asked whether the reason for this apparent difference is a consequence of the very different methodologies used in speech and non-speech studies. We hypothesized that speech and non-speech training would result in a similar pattern of learning if they were trained using the same training regimen. We used a 2 (random vs. blocked pre- and post-testing) × 2 (random vs. blocked training) × 2 (speech vs. non-speech discrimination task) study design, yielding 8 training groups. A further 2 groups acted as untrained controls, tested with either random or blocked stimuli. The speech task required syllable discrimination along 4 minimal-pair continua (e.g., bee-dee), and the non-speech stimuli required duration discrimination around 4 base durations (e.g., 50 ms). Training and testing required listeners to pick the odd-one-out of three stimuli, two of which were the base duration or phoneme continuum endpoint and the third varied adaptively. Training was administered in 9 sessions of 640 trials each, spread over 4–8 weeks. Significant learning was only observed following speech training, with similar learning rates and full generalization regardless of whether training used random or blocked schedules. No learning was observed for duration discrimination with either training regimen. We therefore conclude that the two stimulus classes respond differently to the same training regimen. A reasonable interpretation of the findings is that speech is perceived categorically, enabling learning in either paradigm, while the different base durations are not well-enough differentiated to allow for categorization, resulting in disruption to learning.     

Distractor Evoked Deviations of Saccade Trajectory Are Modulated by Fixation Activity in the Superior Colliculus: Computational and Behavioral Evidence

Previous studies have shown that saccades may deviate towards or away from task irrelevant visual distractors. This observation has been attributed to active suppression (inhibition) of the distractor location unfolding over time: early in time inhibition at the distractor location is incomplete causing deviation towards the distractor, while later in time when inhibition is complete the eyes deviate away from the distractor. In a recent computational study, Wang, Kruijne and Theeuwes proposed an alternative theory that the lateral interactions in the superior colliculus (SC), which are characterized by short-distance excitation and long-distance inhibition, are sufficient for generating both deviations towards and away from distractors. In the present study, we performed a meta-analysis of the literature, ran model simulations and conducted two behavioral experiments to further explore this unconventional theory. Confirming predictions generated by the model simulations, the behavioral experiments show that a) saccades deviate towards close distractors and away from remote distractors, and b) the amount of deviation depends on the strength of fixation activity in the SC, which can be manipulated by turning off the fixation stimulus before or after target onset (Experiment 1), or by varying the eccentricity of the target and distractor (Experiment 2).     

Corticospinal Excitability Preceding the Grasping of Emotion-Laden Stimuli

Evolutionary theories posit that emotions prime organisms for action. This study examined whether corticospinal excitability (CSE) is modulated by the emotional valence of a to-be-grasped stimulus. CSE was estimated based on the amplitude of motor evoked potentials (MEPs) elicited using transcranial magnetic stimulation (TMS) and recorded on the first dorsal interosseous (FDI) muscle. Participants were instructed to grasp (ACTION condition) or just look at (NO-ACTION condition) unpleasant, pleasant and neutral stimuli. TMS pulses were applied randomly at 500 or 250 ms before a go signal. MEP amplitudes were normalized within condition by computing a ratio for the emotion-laden stimuli by reference to the neutral stimuli. A divergent valence effect was observed in the ACTION condition, where the CSE ratio was higher during the preparation to grasp unpleasant compared to pleasant stimuli. In addition, the CSE ratio was lower for pleasant stimuli during the ACTION condition compared to the NO-ACTION condition. Altogether, these results indicate that motor preparation is selectively modulated by the valence of the stimulus to be grasped. The lower CSE for pleasant stimuli may result from the need to refrain from executing an imminent action.     

Effects on discrimination performance of selective attention to tactile features

This study examined selective attention to tactile dimensions by combining a selective cueing paradigm with a test of integrality. In Experiment 1, subjects selectively attended to changes in the frequency or duration of pairs of vibrotactile stimuli and identified the higher frequency or longer duration stimulus. In Experiment 2, using surface gratings in an identical experimental procedure, subjects identified the rougher or longer duration stimulus. In both experiments, greater performance accuracy was found on trials where the cue correctly (valid) predicted the changing dimension, vs incorrectly (invalid) cued or no-cue (neutral) trials. More errors on the invalidly vs neutrally cued trials show the cost of focal attention. Increases in performance on validly vs neutrally cued trials show a benefit of filtering irrelevant stimuli in the cued conditions. Results effectively demonstrate focal attention to tactile features. Tests of integrality, in terms of the effects of correlated change in both dimensions, showed no redundancy gain for either vibrotactile or grating tasks, suggesting that frequency and roughness are separable from stimulus duration. Interference of negative correlated change for frequency but not roughness discriminations may be explained by differences in task difficulty.     

Effects on discrimination performance of selective attention to tactile features

This study examined selective attention to tactile dimensions by combining a selective cueing paradigm with a test of integrality. In Experiment 1, subjects selectively attended to changes in the frequency or duration of pairs of vibrotactile stimuli and identified the higher frequency or longer duration stimulus. In Experiment 2, using surface gratings in an identical experimental procedure, subjects identified the rougher or longer duration stimulus. In both experiments, greater performance accuracy was found on trials where the cue correctly (valid) predicted the changing dimension, vs incorrectly (invalid) cued or no-cue (neutral) trials. More errors on the invalidly vs neutrally cued trials show the cost of focal attention. Increases in performance on validly vs neutrally cued trials show a benefit of filtering irrelevant stimuli in the cued conditions. Results effectively demonstrate focal attention to tactile features. Tests of integrality, in terms of the effects of correlated change in both dimensions, showed no redundancy gain for either vibrotactile or grating tasks, suggesting that frequency and roughness are separable from stimulus duration. Interference of negative correlated change for frequency but not roughness discriminations may be explained by differences in task difficulty.     

Influence of Stimuli Spatial Proximity on a SSVEP-Based BCI Performance

Objective: Steady-State Visual Evoked Potentials based Brain-Computer Interfaces (SSVEP-based BCIs) systems have been shown as promising technology due to their short response time and ease of use. SSVEP-based BCIs use brain responses to a flickering visual stimulus as an input command to an external application or device, and it can be influenced by stimulus properties, signal recording, and signal processing. We aim to investigate the system performance varying the stimuli spatial proximity (a stimulus property).Material and methods: We performed a comparative analysis of two visual interface designs (named cross and square) for an SSVEP-based BCI. The power spectrum density (PSD) was used as feature extraction and the Support Machine Vector (SVM) as classification method. We also analyzed the effects of five flickering frequencies (6.67, 8.57, 10, 12 e 15 Hz) between and within interfaces.Results: We found higher accuracy rates for the flickering frequencies of 10, 12, and 15 Hz. The stimulus of 10 Hz presented the highest SSVEP amplitude response for both interfaces. The system presented the best performance (highest classification accuracy and information transfer rate) using the cross interface (lower visual angle).Conclusion: Our findings suggest that the system has the highest performance in the spatial proximity range from 4° to 13° (visual angle). In addition, we conclude that as the stimulus spatial proximity increases, the interference from other stimuli reduces, and the SSVEP amplitude response decreases, which reduces system accuracy. The inter-stimulus distance is a visual interface parameter that must be chosen carefully to increase the efficiency of an SSVEP-based BCI.     

SSCC TD: A Serial and Simultaneous Configural-Cue Compound Stimuli Representation for Temporal Difference Learning

This paper presents a novel representational framework for the Temporal Difference (TD) model of learning, which allows the computation of configural stimuli – cumulative compounds of stimuli that generate perceptual emergents known as configural cues. This Simultaneous and Serial Configural-cue Compound Stimuli Temporal Difference model (SSCC TD) can model both simultaneous and serial stimulus compounds, as well as compounds including the experimental context. This modification significantly broadens the range of phenomena which the TD paradigm can explain, and allows it to predict phenomena which traditional TD solutions cannot, particularly effects that depend on compound stimuli functioning as a whole, such as pattern learning and serial structural discriminations, and context-related effects.