Role of Prefrontal Cortex in Learning and Generalizing Hierarchical Rules in 8-Month-Old Infants

Abstract

Recent research indicates that adults and infants spontaneously create and generalize hierarchical rule sets during incidental learning. Computational models and empirical data suggest that, in adults, this process is supported by circuits linking prefrontal cortex (PFC) with striatum and their modulation by dopamine, but the neural circuits supporting this form of learning in infants are largely unknown. We used near-infrared spectroscopy to record PFC activity in 8-month-old human infants during a simple audiovisual hierarchical-rule-learning task. Behavioral results confirmed that infants adopted hierarchical rule sets to learn and generalize spoken object-label mappings across different speaker contexts. Infants had increased activity over right dorsal lateral PFC when rule sets switched from one trial to the next, a neural marker related to updating rule sets into working memory in the adult literature. Infants' eye blink rate, a possible physiological correlate of striatal dopamine activity, also increased when rule sets switched from one trial to the next. Moreover, the increase in right dorsolateral PFC activity in conjunction with eye blink rate also predicted infants' generalization ability, providing exploratory evidence for frontostriatal involvement during learning. These findings provide evidence that PFC is involved in rudimentary hierarchical rule learning in 8-month-old infants, an ability that was previously thought to emerge later in life in concert with PFC maturation.

Significance statement: Hierarchical rule learning is a powerful learning mechanism that allows rules to be selected in a context-appropriate fashion and transferred or reused in novel contexts. Data from computational models and adults suggests that this learning mechanism is supported by dopamine-innervated interactions between prefrontal cortex (PFC) and striatum. Here, we provide evidence that PFC also supports hierarchical rule learning during infancy, challenging the current dogma that PFC is an underdeveloped brain system until adolescence. These results add new insights into the neurobiological mechanisms available to support learning and generalization in very early postnatal life, providing evidence that PFC and the frontostriatal circuitry are involved in organizing learning and behavior earlier in life than previously known.

Keywords: development; eye blink rate; frontostriatal circuitry; generalization; prefrontal cortex; rule learning.

Figure 1.

A, Hierarchical rule structure used during the task, which was modeled after Werchan et al. (2015). During the learning task, infants saw face–voice/toy–word mappings that could be grouped into hierarchical rule sets using the faces and voices as higher-order contexts. During the generalization task, infants saw a previously learned rule set now paired with a novel face and voice (RS1-A) and one new toy–word pairing was added to the rule set. During the inference test, infants saw the faces and voices from the learning task paired with the novel toy–word mapping from the generalization task. Infants' looking time to pairings that were consistent versus inconsistent with the hierarchical structure was measured. B, The learning task was split into two 24 s blocks in which the higher-order rule switched from one trial to the next (Switch 1 and Switch 2) and two 24 s blocks in which the higher-order rule stayed the same from one trial to the next (Stay 1 and Stay 2). The order of blocks was counterbalanced.

Figure 2.

A, Sources (letters) and detectors (numbers) were arranged in a lattice pattern and placed inside of a neoprene headband with the lower edge of the headband positioned in line with the Fp1-Fpz-Fp2 line in the international 10–20 system. Red lines represent channels over mPFC and blue lines represent channels over dlPFC. B, Measurement sensitivity to frontal cortex was estimated using AtlasViewer (Aasted et al., 2015), which indicated that the source-detector channels likely targeted a broad area over frontal cortex, including mPFC and dlPFC.

Figure 3.

A, During the inference test, infants' looking times to pairings that were consistent versus inconsistent with the learned rule structures was measured. B, Infants looked significantly longer at the inconsistent pairing, providing evidence that they constructed hierarchical rule sets and used these sets to make inferences about novel pairings. Error bars indicate SEM.

Figure 4.

Infants' eye blink rate was significantly greater during the second rule switch block relative to the first rule switch block during learning. Error bars indicate SEM.

Figure 5.

Right dlPFC activity was greater during the second switch block relative to the second stay block in infants who demonstrated better learning and generalization of the rule set structure, as evidenced by the significant interaction between interval, condition, and learning score. To illustrate this interaction visually, the baseline-corrected change in right dlPFC activity is shown in the 10 infants with the best learning scores (A) and the 10 infants with the worst learning scores (B). Error bars indicate SEM.

Figure 6.

A, Significant cortical activity was observed in channels over right dlPFC (measurement sensitivity map shown) during Switch 2 relative to Stay 2 in infants who demonstrated subsequent transfer of the rule structures. B, Partial regression plot illustrating the relation among right dlPFC activity, eye blink rate, and transfer performance. Results from the regression analysis indicated that a conjunction between eye blink rate and the change in right dlPFC activity (from the beginning to the end of each block) predicted transfer performance during the subsequent inference test. In particular, infants with a higher blink rate combined with a greater change in right dlPFC activity showed better transfer performance.