Emergence of Novel Representations in Primary Motor Cortex and Premotor Neurons during Associative Learning

Abstract

Neurons in the motor areas of cortex play a key role in associating sensory instructions with movements. However, their ability to acquire and maintain representations of novel stimulus features, especially when these features are behaviorally relevant, remains unknown. We investigated neuronal changes in these areas during and after associative learning, by training monkeys on a novel reaching task that required associating target colors with movement directions. Before and after learning, the monkeys performed a well known center-out task. We found that during learning, up to 48% of the neurons developed learning-related responses, differentiating between the associative task and the center-out task, although movement kinematics were the same. After learning, on returning to the center-out task in which color was irrelevant, many of these neurons maintained their response to the associative task; they displayed novel sensitivity to the color of the target that was relevant during learning. These neuronal responses prevailed in both the primary motor cortex and the ventral and dorsal premotor cortices, without degrading the information that the neurons firing carried about movement direction. Our results show that motor cortical neurons can rapidly develop and maintain sensitivities to novel arbitrary sensory features such as color, when such features are behaviorally relevant.

The Representation of Visual and Motor Aspects of Reaching Movements in the Human Motor Cortex

“…There is some evidence that neurons in monkey M1 are sensitive to the location (or other features) of the visual cue (Zhang et al, 1997;Zach et al, 2008;Saleh et al, 2010). However, previous fMRI studies in humans (Toni et al, 1999;Stark and Zohary, 2008;Chouinard and Goodale, 2009), which contained a visual target or a visual cue, did not show any visually induced M1 activation.…”

“…For example, using a visuomotor rotation task, which introduces a constant angular difference between the motor trajectory of the hand and its viewed trajectory on the screen, Alexander and colleagues showed that M1 neurons are sensitive to the target position on the screen (Alexander and Crutcher, 1990;Shen and Alexander, 1997a). Furthermore, the sensitivity of neurons in M1 to sensory stimuli often depends on their functional relevance: when the color of a visual cue carried crucial information to indicate the required hand movement, a considerable fraction of M1 neurons (20%) displayed color sensitivity (Zach et al, 2008).…”

Trial-to-Trial Variability of Single Cells in Motor Cortices Is Dynamically Modified during Visuomotor Adaptation

“…For example, modulation of variability might represent adjustments of the forward model that the brain can use to test different movement plans to minimize on-line corrections. Alternatively, the variability may represent the process selecting the association between an instruction (TO) and a new specific action (movement direction) (Wise et al, 1996;Zach et al, 2008). The association requires few (if any) changes in the kinematics to dynamics transformations since there was no alternation in the relationship between movement and muscle activity.…”

The Neuronal Basis of Long-Term Sensorimotor Learning

“…Psychophysical studies provided evidence for the nature of sensorimotor learning by testing features such as dynamics of acquisition, generalization, and consolidation (Krakauer et al, 1999;Donchin et al, 2003;Caithness et al, 2004). In parallel, physiological studies have demonstrated that neuronal activity in the motor cortex conveys information about the characteristics of the required movement, such as the desired direction (Georgopoulos et al, 1982(Georgopoulos et al, , 1983 and muscle forces (Evarts, 1968), which can change through learning (Mitz et al, 1991;Chen and Wise, 1995;Wise et al, 1996Wise et al, , 1998Gandolfo et al, 2000;Paz et al, 2003;Zach et al, 2008).…”