Neural systems underlying learning and representation of global motion

Abstract

A BSTR ACTWe demonstrate performance-related changes in cortical and cerebellar activity. The largest learning-dependent changes were observed in the anterior lateral cerebellum, where the extent and intensity of activation correlated inversely with psychophysical performance. After learning had occurred (a few minutes), the cerebellar activation almost disappeared; however, it was restored when the subjects were presented with a novel, untrained direction of motion for which psychophysical performance also reverted to chance level. Similar reductions in the extent and intensity of brain activations in relation to learning occurred in the superior colliculus, anterior cingulate, and parts of the extrastriate cortex. The motion direction-sensitive middle temporal visual complex was a notable exception, where there was an expansion of the cortical territory activated by the trained stimulus. Together, these results indicate that the learning and representation of visual motion discrimination are mediated by different, but probably interacting, neuronal subsystems.In previous psychophysical studies of perceptual learning of a direction-of-motion discrimination task we found that the subjects' performance improves with practice over less than 300 trials in a single testing session, is retained over time, and is specific for the particular stimulus attributes (1). Given the time course of minutes over which this learning takes place, the neural substrates of the perceptual learning can be studied by using functional MRI (fMRI) as described here.Until recently, the predominant view of plasticity of cortical maps and of functional properties of neurons in the early levels of cortical sensory processing was that they are specific to early development and are fixed in adulthood. Research over the past 15 years has amply demonstrated that this is not the case. It is now clearly established that cortical maps in the early stages of sensory processing in the adult animal are not fixed, but dynamic throughout life. Lesion studies in different adult mammalian species, including humans, have demonstrated significant neuronal plasticity. When a specific cortical area is deprived of its normal afferent inputs, it reorganizes so that it becomes responsive to inputs that were initially represented only by the surrounding cortex (for a review, see ref.2). Another important form of neural plasticity, known as perceptual learning, relies on changes resulting from practicing stimulus discrimination. These two forms of cortical plasticity are complementary. In the former, there is a peripheral or central reduction of the input, whereas in the latter there is an enrichment of the input (3).Currently, considerable research is aimed toward understanding the relationship between neuronal activity and performance on a task, particularly within the framework of perceptual learning. One proposal is that learning largely implies an increased representation of the trained stimulus, and thus the effects of learning may be manifested as recruitme...

Activations in Visual and Attention-Related Areas Predict and Correlate with the Degree of Perceptual Learning

“…This result suggests that subsequent learning depended on enhanced attention to the task initially, and the reduction of activa- tion in attention-related areas during learning may represent a reduced requirement for attention as the task became easier (Vaina et al, 1998). This may also have contributed to the reduced activations within visual cortex (Kastner et al, 1998).…”

“…The results, when superimposed on retinotopic maps of individual subjects, revealed that the reduced activations were seen as early as V1 but mainly in V3-V4 and beyond, all of which contain populations of neurons that are sensitive to stimulus contrast (Boynton et al, 1999;Reynolds et al, 2000;Gardner et al, 2005;Lu and Roe, 2007). Previous studies reported perceptual learning effects in early visual areas, including V1 and V4, when subjects were trained on fine discriminations of simple visual features, such as orientation and texture (Schiltz et al, 1999;Schoups et al, 2001;Schwartz et al, 2002;Furmanski et al, 2004;Yang and Maunsell, 2004;Sigman et al, 2005;Raiguel et al, 2006), and in motion-sensitive areas MT and MST, when subjects were trained on motion discrimination tasks (Zohary et al, 1994;Vaina et al, 1998). These results, together with ours, suggest that learning occurs in visual areas in which the task-relevant visual information is processed.…”

“…Single-unit recording studies of Yang and Maunsell (2004) and Raiguel et al (2006) examined the activity of neurons in visual cortical area V4 and found sharpened orientation tuning curves after training. Similarly, in motion-sensitive areas MT (middle temporal visual area) and MST (medial superior temporal visual area), Vaina et al (1998) used functional magnetic resonance imaging (fMRI) to demonstrate an expansion of the activation zone (accompanied by the disappearance of activation in other extrastriate visual areas), and Zohary et al (1994) used single-unit recordings to show an increase in neural sensitivity after human and monkey subjects, respectively, were trained on a motion discrimination task.…”

Perceptual learning with perceptions

“…(e.g. Zihl et al 1983;Vaina et al 1998;Tsushima et al 2006;Huxlin et al 2009;Furlan and Schwarzbach 2009) and hence we assume that groups of neurons within this area might respond to stimuli moving in a specified direction. 2 For the purpose of the simulations we considered eight groups or pools of neurons which respond when a substantial amount of dots move coherently into their preferred direction.…”

“…Ball and Sekuler 1987;Vaina et al 1998), and that this ability might even increase without an actual perception (Watanabe et al 2001). Furthermore, neuroimaging studies demonstrated that changes in cortical activations might accompany perceptual learning in general (e.g.…”