Control of the superior colliculus by the lateral prefrontal cortex

Abstract

Several decades of patient, functional imaging and neurophysiological studies have supported a model in which the lateral prefrontal cortex (PFC) acts to suppress unwanted saccades by inhibiting activity in the oculomotor system. However, recent results from combined PFC deactivation and neural recordings of the superior colliculus in monkeys demonstrate that the primary influence of the PFC on the oculomotor system is excitatory, and stands in direct contradiction to the inhibitory model of PFC function. Although erroneous saccades towards a visual stimulus are commonly labelled reflexive in patients with PFC damage or dysfunction, the latencies of most of these saccades are outside of the range of express saccades, which are triggered directly by the visual stimulus. Deactivation and pharmacological manipulation studies in monkeys suggest that response errors following PFC damage or dysfunction are not the result of a failure in response suppression but can best be understood in the context of a failure to maintain and implement the proper task set.

Keywords: eye movements; inhibition; prefrontal cortex; primates.

Figure 1.

Schematic of the inhibitory control model. According to this model, the lateral prefrontal cortex (PFC) inhibits saccade-related activity in the ipsilateral superior colliculus (SC). Because cortical output neurons are excitatory, they have to terminate either on fixation neurons (FN) in the rostral SC or on interneurons (IN) to inhibit the activity of saccade-related neurons (SN) that activate long-lead burst neurons (LLBN) in reticular formation in the opposite hemisphere.

Figure 2.

(a) Temporal activity profile of a population of task-related neurons putative pyramidal neurons in the lateral prefrontal cortex (PFC) contralateral to the stimulus [60] and (b) saccade-related neurons in the superior colliculus (SC) on antisaccade (red/light) and prosaccade (blue/dark) trials when the stimulus is presented into the neuron's response field [61]. Activation waveforms were obtained by convolving each spike with an asymmetric function that resembled a postsynaptic potential [62,63]. Shaded envelopes depict within-subjects standard error of the mean discharge rate. Arrows indicate the mean reaction times of pro- and antisaccades in the two datasets. The onset of significant differences between pro- and antisaccade trials in the populations of PFC and SC neurons is indicated by vertical dashed lines. Onset was determined by bootstrap analyses on data from 10 ms sliding ROC analyses (for details, see [60]). (Online version in colour.)

Figure 3.

Effects of caudal principal sulcus cooling on the activity of saccade-related neurons in the superior colliculus on control (red/light) and cooling (blue/dark) trials. Blue patches indicate the deactivation sites. Activity was combined for correct and error trials (same stimulus location but opposite saccade direction). (a) Activity on antisaccade trials on which the stimulus was presented contralateral to the cooled principal sulcus. Data were obtained in a gap saccade task [68]. (b) Same as (a) but on trials on which the stimulus was presented ipsilateral to the cooled principal sulcus. (c) Activity on prosaccade trials in the bilateral deactivation condition in a task that required monkeys to retain the task instruction for 500–700 ms [67]. (d) Same as (c) but on antisaccade trials. S, stimulus; FP, fixation point. (Online version in colour.)

Figure 4.

Behavioural effects of PFC deactivation. (a) Mean per cent errors for 54 experimental sessions from two monkeys on prosaccade (thick lines) and antisaccade trials (thin lines) on overlap trials (solid lines) in which the coloured fixation stimulus is visible throughout the trial and on memory trials (dashed lines) in which the coloured fixation stimulus changed to a neutral stimulus 500–700 ms prior to stimulus onset. (b) Cumulative distribution of all direction errors in the memory condition on antisaccade trials. (c) Mean per cent errors for 17 experimental sessions from one monkey on gap prosaccade trials (solid line) and gap antisaccade trials (dashed line). (d) Cumulative distribution of all direction errors in the gap condition on antisaccade trials. (e) Mean per cent errors for 12 sessions on antisaccade trials with a short delay of 500–700 ms (solid line) and mean per cent errors for 10 sessions with a long delay of 1000–1200 ms (dashed line) obtained in same the monkey. PRE, period before cooling; COOL, during bilateral cooling of the prefrontal cortex; POST, after cooling.