Plasticity in the Structure of Visual Space

Abstract

Visual space embodies all visual experiences, yet what determines the topographical structure of visual space remains unclear. Here we test a novel theoretical framework that proposes intrinsic lateral connections in the visual cortex as the mechanism underlying the structure of visual space. The framework suggests that the strength of lateral connections between neurons in the visual cortex shapes the experience of spatial relatedness between locations in the visual field. As such, an increase in lateral connection strength shall lead to an increase in perceived relatedness and a contraction in perceived distance. To test this framework through human psychophysics experiments, we used a Hebbian training protocol in which two-point stimuli were flashed in synchrony at separate locations in the visual field, to strengthen the lateral connections between two separate groups of neurons in the visual cortex. After training, participants experienced a contraction in perceived distance. Intriguingly, the perceptual contraction occurred not only between the two training locations that were linked directly by the changed connections, but also between the outward untrained locations that were linked indirectly through the changed connections. Moreover, the effect of training greatly decreased if the two training locations were too close together or too far apart and went beyond the extent of lateral connections. These findings suggest that a local change in the strength of lateral connections is sufficient to alter the topographical structure of visual space.

Keywords: Lateral connections; visual plasticity; visual space.

Graphical abstract

Fig. 1.

Experiment design. Each experiment run contained pretraining testing, training, and posttraining testing sessions. In the training session, we used synchronized, repetitive presentation of two-point stimuli to strengthen the lateral connections between two retinotopically tuned neuronal groups. Because the successful induction of synaptic plasticity requires the presence of direct connections between the two neuronal groups, there should be an optimal separation between the two-point stimuli for changing the lateral connection strength. At longer separation, the two neuronal groups would not be effectively connected; at shorter separation, the two neuronal groups could be partially overlapping; either way, the number of lateral connections involved and the net change in lateral connection strength would be less. In the testing session, we used a match-to-standard protocol to measure the perceived distance. Participants adjusted the physical separation of a dot pair in the untrained hemifield to match the perceived distance of a dot pair in the trained hemifield. The difference between the pre- and posttraining matches was taken to quantify the change in perceived distance and the effect of training.

Fig. 2.

Change in perceived distance depends on training separation. The induction of synaptic plasticity and the change in lateral connection strength should be dependent on the separation between training locations. We measured the effect of training for a range of training separations. We observed a maximal contraction in perceived distance when training at a separation of 4.4 degrees. The contraction declined when training at shorter or longer separations. Black line, group average; shaded area, SEM (n = 30).

Fig. 3.

Change in perceived distance between untrained locations. A change in the strength of lateral connections should affect the perceived distance, not only between the training locations, but also between the untrained locations that span the training locations. We measured the effect of training for a range of testing locations. After training at the optimal separation, the perceived distance between the testing locations at 0.4 and 0.8 degrees outward from the training locations was significantly contracted. Black line, group average with SEM (n = 30); colored lines, individual participants. Paired-sample t tests are shown.