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).

Multiple timescales of learning indicated by changes in evidence-accumulation processes during perceptual decision-making.

Evidence accumulation models have enabled strong advances in our understanding of decision-making, yet their application to examining learning has not been common. Using data from participants completing a dynamic random dot-motion direction discrimination task across four days, we characterized alterations in two components of perceptual decision-making (Drift Diffusion Model drift rate and response boundary). Continuous-time learning models were applied to characterize trajectories of performance change, with different models allowing for varying dynamics. The best-fitting model included drift rate changing as a continuous, exponential function of cumulative trial number. In contrast, response boundary changed within each daily session, but in an independent manner across daily sessions. Our results highlight two different processes underlying the pattern of behavior observed across the entire learning trajectory, one involving a continuous tuning of perceptual sensitivity, and another more variable process describing participants' threshold of when enough evidence is present to act.

Temporal Predictability Modulates Cortical Activity and Functional Connectivity in the Frontoparietal Network in 6-Month-Old Infants.

Despite the abundance of behavioral evidence showing the interaction between attention and prediction in infants, the neural underpinnings of this interaction are not yet well understood. The endogenous attentional function in adults have been largely localized to the frontoparietal network. However, resting-state and neuroanatomical investigations have found that this frontoparietal network exhibits a protracted developmental trajectory and involves weak and unmyelinated long-range connections early in infancy. Can this developmentally nascent network still be modulated by predictions? Here, we conducted the first investigation of infant frontoparietal network engagement as a function of the predictability of visual events. Using functional near-infrared spectroscopy, the hemodynamic response in the frontal, parietal, and occipital lobes was analyzed as infants watched videos of temporally predictable or unpredictable sequences. We replicated previous findings of cortical signal attenuation in the frontal and sensory cortices in response to predictable sequences and extended these findings to the parietal lobe. We also estimated background functional connectivity (i.e., by regressing out task-evoked responses) to reveal that frontoparietal functional connectivity was significantly greater during predictable sequences compared to unpredictable sequences, suggesting that this frontoparietal network may underlie how the infant brain communicates predictions. Taken together, our results illustrate that temporal predictability modulates the activation and connectivity of the frontoparietal network early in infancy, supporting the notion that this network may be functionally available early in life despite its protracted developmental trajectory.

Retinotopic organization of visual cortex in human infants.

Vision develops rapidly during infancy, yet how visual cortex is organized during this period is unclear. In particular, it is unknown whether functional maps that organize the mature adult visual cortex are present in the infant striate and extrastriate cortex. Here, we test the functional maturity of infant visual cortex by performing retinotopic mapping with functional magnetic resonance imaging (fMRI). Infants aged 5-23 months had retinotopic maps, with alternating preferences for vertical and horizontal meridians indicating the boundaries of visual areas V1 to V4 and an orthogonal gradient of preferences from high to low spatial frequencies. The presence of multiple visual maps throughout visual cortex in infants indicates a greater maturity of extrastriate cortex than previously appreciated. The areas showed subtle age-related fine-tuning, suggesting that early maturation undergoes continued refinement. This early maturation of area boundaries and tuning may scaffold subsequent developmental changes.

Evidence of hippocampal learning in human infants.

The hippocampus is essential for human memory.1 The protracted maturation of memory capacities from infancy through early childhood2-4 is thus often attributed to hippocampal immaturity.5-7 The hippocampus of human infants has been characterized in terms of anatomy,8,9 but its function has never been tested directly because of technical challenges.10,11 Here, we use recently developed methods for task-based fMRI in awake human infants12 to test the hypothesis that the infant hippocampus supports statistical learning.13-15 Hippocampal activity increased with exposure to visual sequences of objects when the temporal order contained regularities to be learned, compared to when the order was random. Despite the hippocampus doubling in anatomical volume across infancy, learning-related functional activity bore no relationship to age. This suggests that the hippocampus is recruited for statistical learning at the youngest ages in our sample, around 3 months. Within the hippocampus, statistical learning was clearer in anterior than posterior divisions. This is consistent with the theory that statistical learning occurs in the monosynaptic pathway,16 which is more strongly represented in the anterior hippocampus.17,18 The monosynaptic pathway develops earlier than the trisynaptic pathway, which is linked to episodic memory,19,20 raising the possibility that the infant hippocampus participates in statistical learning before it forms durable memories. Beyond the hippocampus, the medial prefrontal cortex showed statistical learning, consistent with its role in adult memory integration21 and generalization.22 These results suggest that the hippocampus supports the vital ability of infants to extract the structure of their environment through experience.

Optimal, resource-rational or sub-optimal? Insights from cognitive development.

We agree with the authors regarding the utility of viewing cognition as resulting from an optimal use of limited resources. Here, we advocate for extending this approach to the study of cognitive development, which we feel provides particularly powerful insight into the debate between bounded optimality and true sub-optimality, precisely because young children have limited computational and cognitive resources.

Young children combine sensory cues with learned information in a statistically efficient manner: But task complexity matters.

Human adults are adept at mitigating the influence of sensory uncertainty on task performance by integrating sensory cues with learned prior information, in a Bayes-optimal fashion. Previous research has shown that young children and infants are sensitive to environmental regularities, and that the ability to learn and use such regularities is involved in the development of several cognitive abilities. However, it has also been reported that children younger than 8 do not combine simultaneously available sensory cues in a Bayes-optimal fashion. Thus, it remains unclear whether, and by what age, children can combine sensory cues with learned regularities in an adult manner. Here, we examine the performance of 6- to 7-year-old children when tasked with localizing a 'hidden' target by combining uncertain sensory information with prior information learned over repeated exposure to the task. We demonstrate that 6- to 7-year-olds learn task-relevant statistics at a rate on par with adults, and like adults, are capable of integrating learned regularities with sensory information in a statistically efficient manner. We also show that variables such as task complexity can influence young children's behavior to a greater extent than that of adults, leading their behavior to look sub-optimal. Our findings have important implications for how we should interpret failures in young children's ability to carry out sophisticated computations. These 'failures' need not be attributed to deficits in the fundamental computational capacity available to children early in development, but rather to ancillary immaturities in general cognitive abilities that mask the operation of these computations in specific situations.

Noise correlations in the human brain and their impact on pattern classification.

Multivariate decoding methods, such as multivoxel pattern analysis (MVPA), are highly effective at extracting information from brain imaging data. Yet, the precise nature of the information that MVPA draws upon remains controversial. Most current theories emphasize the enhanced sensitivity imparted by aggregating across voxels that have mixed and weak selectivity. However, beyond the selectivity of individual voxels, neural variability is correlated across voxels, and such noise correlations may contribute importantly to accurate decoding. Indeed, a recent computational theory proposed that noise correlations enhance multivariate decoding from heterogeneous neural populations. Here we extend this theory from the scale of neurons to functional magnetic resonance imaging (fMRI) and show that noise correlations between heterogeneous populations of voxels (i.e., voxels selective for different stimulus variables) contribute to the success of MVPA. Specifically, decoding performance is enhanced when voxels with high vs. low noise correlations (measured during rest or in the background of the task) are selected during classifier training. Conversely, voxels that are strongly selective for one class in a GLM or that receive high classification weights in MVPA tend to exhibit high noise correlations with voxels selective for the other class being discriminated against. Furthermore, we use simulations to show that this is a general property of fMRI data and that selectivity and noise correlations can have distinguishable influences on decoding. Taken together, our findings demonstrate that if there is signal in the data, the resulting above-chance classification accuracy is modulated by the magnitude of noise correlations.

Learning and inference using complex generative models in a spatial localization task.

A large body of research has established that, under relatively simple task conditions, human observers integrate uncertain sensory information with learned prior knowledge in an approximately Bayes-optimal manner. However, in many natural tasks, observers must perform this sensory-plus-prior integration when the underlying generative model of the environment consists of multiple causes. Here we ask if the Bayes-optimal integration seen with simple tasks also applies to such natural tasks when the generative model is more complex, or whether observers rely instead on a less efficient set of heuristics that approximate ideal performance. Participants localized a "hidden" target whose position on a touch screen was sampled from a location-contingent bimodal generative model with different variances around each mode. Over repeated exposure to this task, participants learned the a priori locations of the target (i.e., the bimodal generative model), and integrated this learned knowledge with uncertain sensory information on a trial-by-trial basis in a manner consistent with the predictions of Bayes-optimal behavior. In particular, participants rapidly learned the locations of the two modes of the generative model, but the relative variances of the modes were learned much more slowly. Taken together, our results suggest that human performance in a more complex localization task, which requires the integration of sensory information with learned knowledge of a bimodal generative model, is consistent with the predictions of Bayes-optimal behavior, but involves a much longer time-course than in simpler tasks.

Action video game play facilitates the development of better perceptual templates.

The field of perceptual learning has identified changes in perceptual templates as a powerful mechanism mediating the learning of statistical regularities in our environment. By measuring threshold-vs.-contrast curves using an orientation identification task under varying levels of external noise, the perceptual template model (PTM) allows one to disentangle various sources of signal-to-noise changes that can alter performance. We use the PTM approach to elucidate the mechanism that underlies the wide range of improvements noted after action video game play. We show that action video game players make use of improved perceptual templates compared with nonvideo game players, and we confirm a causal role for action video game play in inducing such improvements through a 50-h training study. Then, by adapting a recent neural model to this task, we demonstrate how such improved perceptual templates can arise from reweighting the connectivity between visual areas. Finally, we establish that action gamers do not enter the perceptual task with improved perceptual templates. Instead, although performance in action gamers is initially indistinguishable from that of nongamers, action gamers more rapidly learn the proper template as they experience the task. Taken together, our results establish for the first time to our knowledge the development of enhanced perceptual templates following action game play. Because such an improvement can facilitate the inference of the proper generative model for the task at hand, unlike perceptual learning that is quite specific, it thus elucidates a general learning mechanism that can account for the various behavioral benefits noted after action game play.

Perceptual learning as improved probabilistic inference in early sensory areas.

Extensive training on simple tasks such as fine orientation discrimination results in large improvements in performance, a form of learning known as perceptual learning. Previous models have argued that perceptual learning is due to either sharpening and amplification of tuning curves in early visual areas or to improved probabilistic inference in later visual areas (at the decision stage). However, early theories are inconsistent with the conclusions of psychophysical experiments manipulating external noise, whereas late theories cannot explain the changes in neural responses that have been reported in cortical areas V1 and V4. Here we show that we can capture both the neurophysiological and behavioral aspects of perceptual learning by altering only the feedforward connectivity in a recurrent network of spiking neurons so as to improve probabilistic inference in early visual areas. The resulting network shows modest changes in tuning curves, in line with neurophysiological reports, along with a marked reduction in the amplitude of pairwise noise correlations.

Insights from a simple expression for linear fisher information in a recurrently connected population of spiking neurons.

A simple expression for a lower bound of Fisher information is derived for a network of recurrently connected spiking neurons that have been driven to a noise-perturbed steady state. We call this lower bound linear Fisher information, as it corresponds to the Fisher information that can be recovered by a locally optimal linear estimator. Unlike recent similar calculations, the approach used here includes the effects of nonlinear gain functions and correlated input noise and yields a surprisingly simple and intuitive expression that offers substantial insight into the sources of information degradation across successive layers of a neural network. Here, this expression is used to (1) compute the optimal (i.e., information-maximizing) firing rate of a neuron, (2) demonstrate why sharpening tuning curves by either thresholding or the action of recurrent connectivity is generally a bad idea, (3) show how a single cortical expansion is sufficient to instantiate a redundant population code that can propagate across multiple cortical layers with minimal information loss, and (4) show that optimal recurrent connectivity strongly depends on the covariance structure of the inputs to the network.