Infants' top-down perceptual modulation is specific to own-race faces.

Recent studies have revealed the influence of higher-level cognitive systems in modulating perceptual processing (top-down perceptual modulation) in infancy. However, more research is needed to understand how top-down processes in infant perception contribute to early perceptual development. To this end, this study examined infants' top-down perception of own- and other-race faces to reveal whether top-down modulation is linked to the emergence of perceptual specialization. Infants first learned an association between a sound and faces, with the race of the faces manipulated between groups (own race vs. other race). We then tested infants' face perception across various levels of perceptual difficulty (manipulated by presentation duration) and indexed top-down perception by the change in perception when infants heard the sound previously associated with the face (predictive sound) versus an irrelevant sound. Infants exhibited top-down face perception for own-race faces (Experiment 1). However, we present new evidence that infants did not show evidence of top-down modulation for other-race faces (Experiment 2), suggesting an experience-based specificity of this capacity with more effective top-down modulation in familiar perceptual contexts. In addition, we ruled out the possibility that this face race effect was due to differences in infants' associative learning of the sound and faces between the two groups. This work has important implications for understanding the mechanisms supporting perceptual development and how they relate to top-down perception in infancy.

Visual Perception Is Highly Flexible and Context Dependent in Young Infants: A Case of Top-Down-Modulated Motion Perception.

Top-down modulation is an essential cognitive component in human perception. Despite mounting evidence of top-down perceptual modulation in adults, it is largely unknown whether infants can engage in this cognitive function. Here, we examined top-down modulation of motion perception in 6- to 8-month-old infants (recruited in North America) via their smooth-pursuit eye movements. In four experiments, we demonstrated that infants' perception of motion direction can be flexibly shaped by briefly learned predictive cues when no coherent motion is available. The current findings present a novel insight into infant perception and its development: Infant perceptual systems respond to predictive signals engendered from higher-level learning systems, leading to a flexible and context-dependent modulation of perception. This work also suggests that the infant brain is sophisticated, interconnected, and active when placed in a context in which it can learn and predict.

A Computational Role for Top-Down Modulation from Frontal Cortex in Infancy.

Recent findings have shown that full-term infants engage in top-down sensory prediction, and these predictions are impaired as a result of premature birth. Here, we use an associative learning model to uncover the neuroanatomical origins and computational nature of this top-down signal. Infants were exposed to a probabilistic audiovisual association. We find that both groups (full term, preterm) have a comparable stimulus-related response in sensory and frontal lobes and track prediction error in their frontal lobes. However, preterm infants differ from their full-term peers in weaker tracking of prediction error in sensory regions. We infer that top-down signals from the frontal lobe to the sensory regions carry information about prediction error. Using computational learning models and comparing neuroimaging results from full-term and preterm infants, we have uncovered the computational content of top-down signals in young infants when they are engaged in a probabilistic associative learning.

Using pupillometry to investigate predictive processes in infancy.

Prediction, a prospective cognitive process, is increasingly believed to be crucial for adult cognition and learning. Despite decades of targeted research on prediction in adults, methodological limitations still exist for investigating prediction in infancy. In this article, we argue that pupillometry, or the measurement of pupil size, is an effective method to examine predictive processing in infants and will expand on existing methods (namely looking time and anticipatory eye movements). In particular, we argue that there are three specific features of pupillometry that make it particularly useful for augmenting the investigation of prediction in infancy. First, pupillometry has excellent temporal resolution that will facilitate the differentiation of prediction subcomponents. Second, pupillometry is highly continuous across the life span, allowing researchers to directly compare responses between infants and adults using an identical paradigm. Third, pupillometry can be used in conjunction with other behavioral measures, allowing for different yet complementary results. In addition, we review relevant adult and infant pupillometry studies that will facilitate infancy researchers to adopt this technique. Overall, pupillometry is particularly useful in investigating prediction in infancy and opens up several avenues for developmental research.

Prediction in infants and adults: A pupillometry study.

Adults use both bottom-up sensory inputs and top-down signals to generate predictions about future sensory inputs. Infants have also been shown to make predictions with simple stimuli and recent work has suggested top-down processing is available early in infancy. However, it is unknown whether this indicates that top-down prediction is an ability that is continuous across the lifespan or whether an infant's ability to predict is different from an adult's, qualitatively or quantitatively. We employed pupillometry to provide a direct comparison of prediction abilities across these disparate age groups. Pupil dilation response (PDR) was measured in 6-month olds and adults as they completed an identical implicit learning task designed to help learn associations between sounds and pictures. We found significantly larger PDR for visual omission trials (i.e. trials that violated participants' predictions without the presentation of new stimuli to control for bottom-up signals) compared to visual present trials (i.e. trials that confirmed participants' predictions) in both age groups. Furthermore, a computational learning model that is closely linked to prediction error (Rescorla-Wagner model) demonstrated similar learning trajectories suggesting a continuity of predictive capacity and learning across the two age groups.

Comparing statistical learning across perceptual modalities in infancy: An investigation of underlying learning mechanism(s).

Statistical learning (SL), sensitivity to probabilistic regularities in sensory input, has been widely implicated in cognitive and perceptual development. Little is known, however, about the underlying mechanisms of SL and whether they undergo developmental change. One way to approach these questions is to compare SL across perceptual modalities. While a decade of research has compared auditory and visual SL in adults, we present the first direct comparison of visual and auditory SL in infants (8-10 months). Learning was evidenced in both perceptual modalities but with opposite directions of preference: Infants in the auditory condition displayed a novelty preference, while infants in the visual condition showed a familiarity preference. Interpreting these results within the Hunter and Ames model (1988), where familiarity preferences reflect a weaker stage of encoding than novelty preferences, we conclude that there is weaker learning in the visual modality than the auditory modality for this age. In addition, we found evidence of different developmental trajectories across modalities: Auditory SL increased while visual SL did not change for this age range. The results suggest that SL is not an abstract, amodal ability; for the types of stimuli and statistics tested, we find that auditory SL precedes the development of visual SL and is consistent with recent work comparing SL across modalities in older children.

The blowfish effect: children and adults use atypical exemplars to infer more narrow categories during word learning.

Learners preferentially interpret novel nouns at the basic level ('dog') rather than at a more narrow level ('Labrador'). This 'basic-level bias' is mitigated by statistics: children and adults are more likely to interpret a novel noun at a more narrow label if they witness 'a suspicious coincidence' - the word applied to three exemplars of the same narrow category. Independent work has found that exemplar typicality influences learners' inferences and category learning. We bring these lines of work together to investigate whether the content (typicality) of a single exemplar affects the level of interpretation of words and whether an atypicality effect interacts with input statistics. Results demonstrate that both four- to five-year-olds and adults tend to assign a narrower interpretation to a word if it is exemplified by an atypical category member. This atypicality effect is roughly as strong as, and independent of, the suspicious coincidence effect, which is replicated.

The Lateral Occipital Cortex Is Selective for Object Shape, Not Texture/Color, at Six Months.

Understanding how the human visual system develops is crucial to understanding the nature and organization of our complex and varied visual representations. However, previous investigations of the development of the visual system using fMRI are primarily confined to a subset of the visual system (high-level vision: faces, scenes) and relatively late in visual development (starting at 4-5 years of age). The current study extends our understanding of human visual development by presenting the first systematic investigation of a mid-level visual region [the lateral occipital cortex (LOC)] in a population much younger than has been investigated in the past: 6 month olds. We use functional near-infrared spectroscopy (fNIRS), an emerging optical method for recording cortical hemodynamics, to perform neuroimaging with this very young population. Whereas previous fNIRS studies have suffered from imprecise neuroanatomical localization, we rely on the most rigorous MR coregistration of fNIRS data to date to image the infant LOC. We find surprising evidence that at 6 months the LOC has functional specialization that is highly similar to adults. Following Cant and Goodale (2007), we investigate whether the LOC tracks shape information and not other cues to object identity (e.g., texture/material). This finding extends evidence of LOC specialization from early childhood into infancy and earlier than developmental trajectories of high-level visual regions.SIGNIFICANCE STATEMENT Understanding visual development is crucial to understanding the nature of visual representations in the human brain. Previous studies of visual development have investigated children (4 years and older) and high-level visual areas. This study expands our knowledge of visual development by investigating the functional development of mid-level vision [lateral occipital cortex (LOC)] early in infancy. We find surprisingly adult-like functional specialization of the LOC by 6 months of age: infants exhibit shape selectivity, but not object selectivity, in this region.

Top-down modulation in the infant brain: Learning-induced expectations rapidly affect the sensory cortex at 6 months.

Recent theoretical work emphasizes the role of expectation in neural processing, shifting the focus from feed-forward cortical hierarchies to models that include extensive feedback (e.g., predictive coding). Empirical support for expectation-related feedback is compelling but restricted to adult humans and nonhuman animals. Given the considerable differences in neural organization, connectivity, and efficiency between infant and adult brains, it is a crucial yet open question whether expectation-related feedback is an inherent property of the cortex (i.e., operational early in development) or whether expectation-related feedback develops with extensive experience and neural maturation. To determine whether infants' expectations about future sensory input modulate their sensory cortices without the confounds of stimulus novelty or repetition suppression, we used a cross-modal (audiovisual) omission paradigm and used functional near-infrared spectroscopy (fNIRS) to record hemodynamic responses in the infant cortex. We show that the occipital cortex of 6-month-old infants exhibits the signature of expectation-based feedback. Crucially, we found that this region does not respond to auditory stimuli if they are not predictive of a visual event. Overall, these findings suggest that the young infant's brain is already capable of some rudimentary form of expectation-based feedback.

The emergence of top-down, sensory prediction during learning in infancy: A comparison of full-term and preterm infants.

Prematurity alters developmental trajectories in preterm infants even in the absence of medical complications. Here, we use fNIRS and learning tasks to probe the nature of the developmental differences between preterm and full-term born infants. Our recent work has found that prematurity disrupts the ability to engage in top-down sensory prediction after learning. We now examine the neural changes during the learning that precede prediction. In full-terms, we found modulation of all cortical regions examined during learning (temporal, frontal, and occipital). By contrast, preterm infants had no evidence of neural changes in the occipital lobe selectively. This is striking as the learning task leads to the emergence of visual prediction. Moreover, the shape of individual infants' occipital lobe trajectories (regardless of prematurity) predicts subsequent visual prediction abilities. These results suggest that modulation of sensory cortices during learning is closely related to the emergence of top-down signals and further indicates that developmental differences in premature infants may be associated with deficits in top-down processing.

Neural Signatures of Spatial Statistical Learning: Characterizing the Extraction of Structure from Complex Visual Scenes.

Behavioral evidence has shown that humans automatically develop internal representations adapted to the temporal and spatial statistics of the environment. Building on prior fMRI studies that have focused on statistical learning of temporal sequences, we investigated the neural substrates and mechanisms underlying statistical learning from scenes with a structured spatial layout. Our goals were twofold: (1) to determine discrete brain regions in which degree of learning (i.e., behavioral performance) was a significant predictor of neural activity during acquisition of spatial regularities and (2) to examine how connectivity between this set of areas and the rest of the brain changed over the course of learning. Univariate activity analyses indicated a diffuse set of dorsal striatal and occipitoparietal activations correlated with individual differences in participants' ability to acquire the underlying spatial structure of the scenes. In addition, bilateral medial-temporal activation was linked to participants' behavioral performance, suggesting that spatial statistical learning recruits additional resources from the limbic system. Connectivity analyses examined, across the time course of learning, psychophysiological interactions with peak regions defined by the initial univariate analysis. Generally, we find that task-based connectivity with these regions was significantly greater in early relative to later periods of learning. Moreover, in certain cases, decreased task-based connectivity between time points was predicted by overall posttest performance. Results suggest a narrowing mechanism whereby the brain, confronted with a novel structured environment, initially boosts overall functional integration and then reduces interregional coupling over time.

Tracing trajectories of audio-visual learning in the infant brain.

Although infants begin learning about their environment before they are born, little is known about how the infant brain changes during learning. Here, we take the initial steps in documenting how the neural responses in the brain change as infants learn to associate audio and visual stimuli. Using functional near-infrared spectroscopy (fNRIS) to record hemodynamic responses in the infant cortex (temporal, occipital, and frontal cortex), we find that across the infant brain, learning is characterized by an increase in activation followed by a decrease. We take this U-shaped response as evidence of repetition enhancement during early stages of learning and repetition suppression during later stages, a result that mirrors the Hunter and Ames model of infant visual preference. Furthermore, we find that the neural response to violations of the learned associations can be predicted by the shape of the learning curve in temporal and occipital cortex. These data provide the first look at the shape of the neural response during audio-visual associative learning in infancy establishing that diverse regions of the infant brain exhibit systematic changes across the time-course of learning.

Hemodynamic correlates of cognition in human infants.

Over the past 20 years, the field of cognitive neuroscience has relied heavily on hemodynamic measures of blood oxygenation in local regions of the brain to make inferences about underlying cognitive processes. These same functional magnetic resonance imaging (fMRI) and functional near-infrared spectroscopy (fNIRS) techniques have recently been adapted for use with human infants. We review the advantages and disadvantages of these two neuroimaging methods for studies of infant cognition, with a particular emphasis on their technical limitations and the linking hypotheses that are used to draw conclusions from correlational data. In addition to summarizing key findings in several domains of infant cognition, we highlight the prospects of improving the quality of fNIRS data from infants to address in a more sophisticated way how cognitive development is mediated by changes in underlying neural mechanisms.

Gaining knowledge mediates changes in perception (without differences in attention): A case for perceptual learning.

Firestone & Scholl (F&S) assert that perceptual learning is not a top-down effect, because experience-mediated changes arise from familiarity with the features of the object through simple repetition and not knowledge about the environment. Emberson and Amso (2012) provide a clear example of perceptual learning that bypasses the authors' "pitfalls" and in which knowledge, not repeated experience, results in changes in perception.

Combining fMRI and behavioral measures to examine the process of human learning.

Prior to the advent of fMRI, the primary means of examining the mechanisms underlying learning were restricted to studying human behavior and non-human neural systems. However, recent advances in neuroimaging technology have enabled the concurrent study of human behavior and neural activity. We propose that the integration of behavioral response with brain activity provides a powerful method of investigating the process through which internal representations are formed or changed. Nevertheless, a review of the literature reveals that many fMRI studies of learning either (1) focus on outcome rather than process or (2) are built on the untested assumption that learning unfolds uniformly over time. We discuss here various challenges faced by the field and highlight studies that have begun to address them. In doing so, we aim to encourage more research that examines the process of learning by considering the interrelation of behavioral measures and fMRI recording during learning.

Longitudinal assessments of functional near-infrared spectroscopy background functional connectivity in low- and middle-income infants during a social cognition task.

Shortly after birth, human infants demonstrate behavioral selectivity to social stimuli. However, the neural underpinnings of this selectivity are largely unknown. Here, we examine patterns of functional connectivity to determine how regions of the brain interact while processing social stimuli and how these interactions change during the first 2 years of life. Using functional near-infrared spectroscopy (fNIRS), we measured functional connectivity at 6 (n = 147) and 24 (n = 111) months of age in infants from Bangladesh who were exposed to varying levels of environmental adversity (i.e., low- and middle-income cohorts). We employed a background functional connectivity approach that regresses out the effects of stimulus-specific univariate responses that are believed to affect functional connectivity. At 6 months, the two cohorts had similar fNIRS patterns, with moderate connectivity estimates for regions within and between hemispheres. At 24 months, the patterns diverged for the two cohorts. Global (brain-wide) connectivity estimates increased from 6 to 24 months for the low-income cohort and decreased for the middle-income (MI) cohort. In particular, connectivity estimates among regions of interest within the right hemisphere decreased for the MI cohort, providing evidence of neural specialization by 2 years of age. These findings provide insights into the impact of early environmental influences on functional brain development relevant to the processing of social stimuli. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Towards imaging the infant brain at play.

Infants' first-person experiences are crucial to early cognitive and neural development. To a vast extent, these early experiences involve play, which in infancy takes the form of object exploration. While at the behavioral level infant play has been studied both using specific tasks and in naturalistic scenarios, the neural correlates of object exploration have largely been studied in highly controlled task settings. These neuroimaging studies did not tap into the complexities of everyday play and what makes object exploration so important for development. Here, we review selected infant neuroimaging studies, spanning from typical, highly controlled screen-based studies on object perception to more naturalistic designs and argue for the importance of studying the neural correlates of key behaviors such as object exploration and language comprehension in naturalistic settings. We suggest that the advances in technology and analytic approaches allow measuring the infant brain at play with the use of functional near-infrared spectroscopy (fNIRS). Naturalistic fNIRS studies offer a new and exciting avenue to studying infant neurocognitive development in a way that will draw us away from our laboratory constructs and into an infant's everyday experiences that support their development.

The Influence of Memory on Visual Perception in Infants, Children, and Adults.

Perception is not an independent, in-the-moment event. Instead, perceiving involves integrating prior expectations with current observations. How does this ability develop from infancy through adulthood? We examined how prior visual experience shapes visual perception in infants, children, and adults. Using an identical task across age groups, we exposed participants to pairs of colorful stimuli and implicitly measured their ability to discriminate relative saturation levels. Results showed that adult participants were biased by previously experienced exemplars, and exhibited weakened in-the-moment discrimination between different levels of saturation. In contrast, infants and children showed less influence of memory in their perception, and they actually outperformed adults in discriminating between current levels of saturation. Our findings suggest that as humans develop, their perception relies more on prior experience and less on current observation.

Learning to sample: eye tracking and fMRI indices of changes in object perception.

We used an fMRI/eye-tracking approach to examine the mechanisms involved in learning to segment a novel, occluded object in a scene. Previous research has suggested a role for effective visual sampling and prior experience in the development of mature object perception. However, it remains unclear how the naive system integrates across variable sampled experiences to induce perceptual change. We generated a Target Scene in which a novel occluded Target Object could be perceived as either "disconnected" or "complete." We presented one group of participants with this scene in alternating sequence with variable visual experience: three Paired Scenes consisting of the same Target Object in variable rotations and states of occlusion. A second control group was presented with similar Paired Scenes that did not incorporate the Target Object. We found that, relative to the Control condition, participants in the Training condition were significantly more likely to change their percept from "disconnected" to "connected," as indexed by pretraining and posttraining test performance. In addition, gaze patterns during Target Scene inspection differed as a function of variable object exposure. We found increased looking to the Target Object in the Training compared with the Control condition. This pattern was not restricted to participants who changed their initial "disconnected" object percept. Neuroimaging data suggest an involvement of the hippocampus and BG, as well as visual cortical and fronto-parietal regions, in using ongoing regular experience to enable changes in amodal completion.

Cognitive development: Looking for perceptual awareness in human infants.

The extent to which young human infants are conscious, in the sense of being perceptually aware of their environment, has been long debated. A new study has revealed that infants do exhibit a key signature of consciousness - the attentional blink - but this early consciousness changes with age.