Circuit Mechanisms of Sensorimotor Learning

Hiroshi Makino, Eun Jung Hwang, Nathan G. Hedrick, Takaki Komiyama
2016 Neuron  
2 SUMMARY 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 in 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
more » ... nsory stimuli. Associative learning and the initial phase of motor skill learning are ensured by feedbackbased 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. Many of our behaviors are modified through sensorimotor learning. Here we broadly define sensorimotor learning as an improvement in one's ability to interact with the environment by interpreting the sensory world and responding to it with the motor system. Let's take an example of braking the car while driving in traffic. To perfect this task, one needs to learn the skill to accurately estimate the flow of traffic (perceptual learning; novices tend to focus on the car in front of them, while experts can selectively use a more diverse set of cues). When one identifies the slowing of the traffic, the visual information initiates a motor program to brake the car (associative learning). They also improve the skill of manipulating the brake smoothly (motor skill learning; try braking with your left foot in an empty parking lot-you'll be surprised.). As illustrated by this example, even a relatively simple behavior involves a multi-level learning process. Accordingly, this review discusses neural changes during sensorimotor learning inthese three hierarchical levels.We note, however,that these levels are closely intertwined with each other and often occur simultaneously. Therefore some mechanisms are likely shared across these levels. An unfortunateconsequence of the broad scope of this review is that many studies or even systems that deserve attention had to be excluded. Despite this compromise, we hope that the broad scope helps us to underscore thedistinctrequirements of each step, which providedistinct constraints on the underlying neural mechanisms (Figure 1 ). Sensory Perceptual Learning Learning of sensorimotor behavior involves selective extraction and efficient processing of sensory information to generate an appropriate action. At the sensory processing stage, rich and multiplex information in the environment is transmitted to the sensory organs where attributes of sensory stimuli are transduced to electrical signals, such as action potentials. As the transduced signal reaches the central nervous system, cognitive factors actively determine what is sampled and what is ignored in the environment. In this vein, the perceptual stage of sensorimotor learning is a process of establishing optimal representations of external stimuli that are deemed to be meaningful, a process known as perceptual learning. This process involves changes in response properties of individualand populations of neurons. In this section, we review recent attempts to understand dynamic changes in sensory representations during perceptual learning, and discuss how these changes are implemented through alterations in operation modes of the underlying circuit. 3 Nature of physiological changes during perceptual learning Despite decades of research, there is still a controversy as to where in the brain neurons change their response properties with perceptual enhancement during sensorimotorlearning and whether and how such changes are causally linked to behavioral improvement. Experiments in visual psychophysics demonstrated that the improved perceptual ability is restrictedto the trained stimulus feature (e.g. orientation) as well as the location in visual space. These results are often interpreted as evidence for the involvement of early stages of cortical visual processing, where neurons are highly selective to physical attributes of visual stimuli, have relatively small receptive fields, and the retinotopic organization is preserved. However, recent experiments using a newly developed double-training paradigm challenged this notion by demonstrating that the feature discrimination (e.g. contrast) abilitycan be transferred to a new retinal location ifsubjects were primed at the second location with a task-irrelevant feature (e.g. orientation) (Xiao et al., 2008) . This observationindicates that perceptual learning may also involve changes in non-retinotopichigher brain areas.
doi:10.1016/j.neuron.2016.10.029 pmid:27883902 pmcid:PMC5131723 fatcat:arc2dhec5vb5bbmuryz3jxjd7u