Circuit Mechanisms of Sensorimotor Learning

Abstract

The relationship between the brain and the environment is flexible, forming the foundation for our ability to learn. Here we review the current state of our understanding of the modifications in the sensorimotor pathway related to sensorimotor learning. We divide the process into three hierarchical levels with distinct goals: (1) sensory perceptual learning, (2) sensorimotor associative learning, and (3) motor skill learning. Perceptual learning optimizes the representations of important sensory stimuli. Associative learning and the initial phase of motor skill learning are ensured by feedback-based mechanisms that permit trial-and-error learning. The later phase of motor skill learning may primarily involve feedback-independent mechanisms operating under the classic Hebbian rule. With these changes under distinct constraints and mechanisms, sensorimotor learning establishes dedicated circuitry for the reproduction of stereotyped neural activity patterns and behavior.

Figure 1

Three hierarchical levels of sensorimotor learning and their unique tasks.

Figure 2. Emerging principles and changes in the circuit operation during perceptual learning

(A) Changes in neural activity during perceptual learning. Left, changes in single neuron activity. Perceptual learning could involve changes in the tuning of individual neurons by increasing its sharpness or gain, or shifting its peak. Right, changes in population activity. Perceptual learning could enhance discriminability of stimuli by decreasing the trial-by-trial response fluctuations (σ), increasing the distance between mean responses (d) or changing noise correlations. Individual dots indicate single trials. Note that the changes in fluctuations and distance can be achieved by independent changes of single neurons, while noise correlation changes would require a coordination across neurons. (B) Perceptual learning could involve changes in the circuit operation. Learning-dependent suppression of distal dendritic inhibition (top) or perisomatic inhibition (bottom) could enhance the impact of top-down processing or the gain of principal neurons, respectively.

Figure 3. Circuit models of sensorimotor associative learning

(A) In this model, sensorimotor association is initially executed by dopamine-dependent plasticity to strengthen the corticostriatal synapses in the basal ganglia carrying specific sensory inputs (‘1’). The downstream pathway drives specific motor responses via PFC (blue). The basal ganglia output to PFC also strengthens sensory input synapses in PFC (‘2’), which subsequently forms a pathway from sensory to prefrontal to motor cortices, bypassing the basal ganglia (green). Further training creates direct cortico-cortical pathways between sensory and motor cortices, via coincidental activation-dependent plasticity (red, ‘3’). (B) Alternative hypothesis: The basal ganglia output to PFC provides a teaching signal, without driving specific motor responses. During the exploration phase of learning, striatal neurons that receive convergent inputs carrying specific sensory and motor information undergo plasticity based on the dopamine prediction error signal (left). This association-specific activity in the basal ganglia provides a teaching signal for PFC neurons that drive the specific motor program to strengthen the synapses carrying the specific sensory information (right). Grey boxes denote the sites of plasticity. In this model, learning is behaviorally evident only after the plasticity in PFC.

Figure 4. Hierarchical mechanisms of circuit modification shape the formation of novel motor skills

(A) During the early phases of learning, the system explores a variety of behavioral options, which coincides with an expansion of the neuronal ensemble size in the motor cortex. (B) Favorable outcomes reinforce a corresponding population of cells, shifting the mean behavior in the process. (C) The repetition of the selected behavior drives Hebbian plasticity in the associated population of cells, eventually resulting in a refined ensemble and highly stereotyped behavior.