Visual information processing in the absence of pulvinar input

Abstract

Pulvinar is the largest thalamic nucleus in primates, having expanded in proportion to neocortex through evolution. Its well-differentiated sub-nuclei have reciprocal connections with different visual cortical areas. Lateral pulvinar (PL) receives input from layer 5 of primary visual cortex (V1) and projects to supragranular layers 1–3 of V1 which, in turn, send outputs to extrastriate ventral visual stream. We studied the effect of PL inactivation on neural activities in supragranular layers of V1 in anesthetized, paralyzed primates (Otolemur garnettii, N = 3). V1 responses to drifting sinusoidal gratings were recorded using a 100-electrode array implanted in supragranular layers. Muscimol was injected in retinotopically matched region of PL. PL inactivation resulted in an almost complete loss of stimulus-driven activity in 95% of all V1 cells studied (N = 164). Despite this overall loss in activity, intriguing changes to the phasic component of the stimulus-driven response were noticeable. Across all orientations, the average instantaneous spike rate of the phasic response to stimulus onset was 4.0 times that of the maintained response before PL inactivation, but decreased to 1.3 after inactivation. Near the preferred orientation, a selective suppression of activity below the maintained response was noticed instead of the phasic increase in activity. This suppression was significant in 95% of units (Rank-Sum, P < 0.01). V1 neurons with partially overlapping receptive fields with inactivated PL neurons showed a significant sustained component in their stimulus-driven activity but without the transient phasic component. Sham injection 500 μm above PL obtained no changes in V1 responses. Thus, PL inactivation profoundly affects activities in the “output” layers of V1. Decreased activity and the strong suppression of the phasic component of stimulus-driven response in the “output” layer neurons could be potential mechanisms for gating the flow of information from V1 to the ventral stream and for bottom-up, stimulus-driven modulation of attention and visual salience.

NIH EY01778.