Top–Down Attentional Deficits in Macaques with Lesions of Lateral Prefrontal Cortex

Abstract

Brain imaging, electrical stimulation, and neurophysiological studies have all implicated the prefrontal cortex (PFC) in the top-down control of attention. Specifically, feedback from PFC has been proposed to bias activity in visual cortex in favor of attended stimuli over irrelevant distracters. To identify which attentional functions are critically dependent on PFC, we removed PFC unilaterally in combination with transection of the corpus callosum and anterior commissure in two macaques. In such a preparation, the ipsilesional hemisphere is deprived of top-down feedback from PFC to visual cortex, and the contralesional hemisphere can serve as an intact normal control. Monkeys were trained to fixate a central cue and discriminate the orientation of a colored target grating presented among colored distracter gratings in either the hemifield affected by the PFC lesion or the normal control hemifield. Locations of the targets and distracters were varied, and the color of the central cue specified the color of the target on each trial. The behavioral response was a bar release, and thus attentional impairments could be distinguished from impaired oculomotor control. When the cue was held constant for many trials, task performance in the affected hemifield was nearly normal. However, the monkeys were severely impaired when the cue was switched frequently across trials. The monkeys were unimpaired in a pop-out task with changing targets that did not require top-down attentional control. The PFC thus appears to play a critical role in the ability to flexibly reallocate attention on the basis of changing task demands.

Prefrontal cortex and basal ganglia contributions to visual working memory

“…These results suggest that the PFC plays a broader role in executive functioning including both top-down attentional control and VWM maintenance, whereas the BG are more directly related to global VWM maintenance processes, extending the role of the BG outside the motor domain. Several studies have reported VWM deficits after lateral PFC damage (1)(2)(3). In contrast, BG lesions lead to a VWM behavioral impairment associated with maintenance deficits despite intact attention mechanisms.…”

“…In essence, we construct and hold a model of the visual world and compare that model against subsequent inputs from the external world. VWM relies upon an intact and functioning prefrontal cortex (PFC), and damage to this region, such as from stroke, causes VWM impairments (1)(2)(3). However, cognitive processes do not localize to specific brain regions per se and a behavior as complex as VWM recruits a distributed network of cortical and subcortical structures (4)(5)(6)(7)(8), including the basal ganglia (BG) (9,10) and visual extrastriate regions (11)(12)(13).…”

“…For example, because PFC lesions lead to working memory deficits, the PFC can be said to play an important, necessary role in working memory networks. Research has shown that unilateral PFC lesions cause lateralized deficits in top-down modulation of visual attention (44,45). These deficits manifest as errors in target detection specifically to targets that appear in the contralesional hemifield.…”

Attentional Modulation of Alpha Oscillations in Macaque Inferotemporal Cortex

“…Whether and how attention modulates ongoing brain activity when it is deployed in advance of sensory stimulation has also attracted increased research interest (Kastner et al, 1999;Driver and Frith, 2000;Pasternak and Greenlee, 2005;Procyk and Goldman-Rakic, 2006;Fuster, 2008). This internally generated expectancy state improves behavioral performance by shortening reaction time and reducing the number of errors and is thought to be implemented by top-down control mechanisms (Knight et al, 1999;Hopfinger et al, 2000;Miller, 2000;Engel et al, 2001;LaBerge, 2005;Buschman and Miller, 2007;Rossi et al, 2007;Fuster, 2008;Gregoriou et al, 2009).…”

Lesions of the basal ganglia and frontal lobe promote differential impairment to working memory and learning ability

“…Neurocomputational models of basal ganglia function has shown us that this model can select the action or make the frontal cortical express a reward or to a correct feedback, reducing the occurrence of errors or negative feedback [7]. The frontal lobe is the most advanced part offound that a visual working memory can be impaired if prefrontal cortex is damaged [10,11]. The prefrontal cortex plays an important role in encode, update and maintain the working memory task context [12].…”