Spatial Updating in Monkey Superior Colliculus in the Absence of the Forebrain Commissures: Dissociation Between Superficial and Intermediate Layers

Abstract

In previous studies, we demonstrated that the forebrain commissures are the primary pathway for remapping from one hemifield to the other. Nonetheless, remapping in lateral intraparietal cortex (LIP) across hemifield is still present in split brain monkeys. This finding indicates that a subcortical structure must contribute to remapping. The primary goal of the current study was to characterize remapping activity in the superior colliculus in intact and split brain monkeys. We recorded neurons in both the superficial and intermediate layers of the SC. We found that across-hemifield remapping was reduced in magnitude and delayed compared with within-hemifield remapping in the intermediate layers of the SC in split brain monkeys. These results mirror our previous findings in area LIP. In contrast, we found no difference in the magnitude or latency for within- compared with across-hemifield remapping in the superficial layers. At the behavioral level, we compared the performance of the monkeys on two conditions of a double-step task. When the second target remained within a single hemifield, performance remained accurate. When the second target had to be updated across hemifields, the split brain monkeys' performance was impaired. Remapping activity in the intermediate layers was correlated with the accuracy and latency of the second saccade during the across-hemifield trials. Remapping in the superficial layers was correlated with latency of the second saccade during the within- and across-hemifield trials. The differences between the layers suggest that different circuits underlie remapping in the superficial and intermediate layers of the superior colliculus.

Neurons in cortical area MST remap the memory trace of visual motion across saccadic eye movements

“…Another possibility is that MST neurons receive visual information in the postsaccadic RF (or future RF) before the time of a saccade. This so-called presaccadic or predictive remapping of RFs has been described in LIP (1,15,16), FEF (2, 6), SC (17)(18)(19), and some areas of the prestriate cortex (3,20). In these areas, neurons that had postsaccadic visual memory responses but not predictive remapping were also recorded (3,(21)(22)(23).…”

Excitatory Synaptic Feedback from the Motor Layer to the Sensory Layers of the Superior Colliculus

“…If the orthodromic component contributes to this lateral spread then the neurons would have to be excitatory, and either have extensive intralaminar projections or activate other neighboring excitatory cells with extensive projections. Three classes of neurons within the superficial SC have been identified as excitatory: wide-field vertical cells, narrow-field vertical cells, and marginal cells (Langer and Lund, 1974;Albano et al, 1979;Mooney et al, 1988;Lee, 1993, 1997;Lee et al, 2001;Chomsung et al, 2008;Isa and Hall, 2009). Marginal cells are located within the stratum zonale, at sites more dorsal than our voltage imaging and patch-clamp results suggest.…”

“…For voltage imaging experiments slices were stained for 45 min with 0.05 mg/ml RH482 (synthesized in this laboratory) at room temperature. Imaging was performed with instrumentation described previously (Wu and Cohen, 1993;Chang and Jackson, 2006;Vokoun et al, 2010). A 464 channel fiber-optic photodiode camera with hexagonal geometry collected light and amplified signals to 5 V/nA of photocurrent.…”

“…Signals were digitized at a frame rate of 5 kHz using a DAP5200 data acquisition board (Microstar Laboratories) and read into a PC. Data acquisition and stimulation were all controlled by a PC running a computer program developed in this laboratory (Chang and Jackson, 2006). Slices were illuminated with a 100 W tungsten-halogen bulb driven by a Kepco ATE 36 -30 power supply.…”

“…This result led to the proposal of a corollary discharge that propagated upward to the superficial layers to enhance the discharge of sensory neurons. Enhancement has since been found in many brain regions (Wurtz and Mohler, 1976a;Hikosaka and Wurtz, 1983;Moran and Desimone, 1985;Boch, 1986;Colby et al, 1996;Lamme et al, 2000;Li and Basso, 2008), but a direct excitatory pathway from SC motor layers to sensory layers has yet to be described. Here, we used voltage imaging and patch-clamp recording in slices of the rodent SC to obtain the first evidence that the motor layer in the SC sends direct excitatory inputs to superficial layer sensory neurons.…”