Unilateral Prefrontal Lesions Impair Memory-Guided Comparisons of Contralateral Visual Motion

Abstract

The contribution of the lateral prefrontal cortex (LPFC) to working memory is the topic of active debate. On the one hand, it has been argued that the persistent delay activity in LPFC recorded during some working memory tasks is a reflection of sensory storage, the notion supported by some lesion studies. On the other hand, there is emerging evidence that the LPFC plays a key role in the maintenance of sensory information not by storing relevant visual signals but by allocating visual attention to such stimuli. In this study, we addressed this question by examining the effects of unilateral LPFC lesions during a working memory task requiring monkeys to compare directions of two moving stimuli, separated by a delay. The lesions resulted in impaired thresholds for contralesional stimuli at longer delays, and these deficits were most dramatic when the task required rapid reallocation of spatial attention. In addition, these effects were equally pronounced when the remembered stimuli were at threshold or moved coherently. The contralesional nature of the deficits points to the importance of the interactions between the LPFC and the motion processing neurons residing in extrastriate area MT. Delay-specificity of the deficit supports LPFC involvement in the maintenance stage of the comparison task. However, because this deficit was independent of stimulus features giving rise to the remembered direction and was most pronounced during rapid shifts of attention, its role is more likely to be attending and accessing the preserved motion signals rather than their storage.

A Source for Feature-Based Attention in the Prefrontal Cortex

“…Previous studies showed that when attention to a cue or stimulus is repeated for many trials, the effects of PFC lesions on attention are greatly reduced (Pasternak et al, 2015; Rossi et al, 2007). We therefore repeated the inactivation of VPA in six additional sessions (three in each monkey) using a blocked design, in which the target cue remained the same in blocks of 20 consecutive trials.…”

Human Dorsolateral Prefrontal Cortex Is Not Necessary for Spatial Working Memory

“…Because Superior 124 132 111 111 122 81 36 3 19 34 25 21 dlPFC 2 Average 106 110 92 111 108 62 16 0 3 2 1 1 dlPFC 3 Average 100 122 94 92 83 64 32 5 50 45 55 25 Excluded because of failure to maintain central fixation when the memory cue appeared in the periphery for a minimum of 50 trials. (Greve, 2001), which is a well-established measure of concept formation and problem solving and is sensitive to "executive" dysfunction following PFC damage (Milner, 1963;Drewe, 1974;Stuss et al, 2000). The test yields several measures of performance, such as the number of completed categories, the number of perseverative and nonperseverative errors, conceptual level responses (measure of insight into sorting principles), and learning to learn (change in conceptual efficiency across the changing categories).…”

“…This controversy has existed for decades (Curtis and D'Esposito, 2004) and continues to drive theoretical questions about the role of the PFC in WM (Sreenivasan et al, 2014;D'Esposito and Postle, 2015). For instance, research questions whether the PFC actively stores WM representations or directs attention to representations stored in sensory cortices (Lebedev et al, 2004;Emrich et al, 2013;Ester et al, 2015;Pasternak et al, 2015). In the current study, our goal was to resolve the discrepancies between the prevailing animal model of human WM and evidence from human neuroimaging studies (Fig.…”

Mnemonic Encoding and Cortical Organization in Parietal and Prefrontal Cortices

“…Historically, persistent activity in the frontoparietal cortex has been viewed as the substrate in which remembered information is stored (Funahashi et al, 1989;Colby et al, 1996;Chafee and Goldman-Rakic, 1998;Rainer et al, 1998;Romo et al, 1999;Ester et al, 2015). However, more recent work has suggested that this activity reflects the coordination with sensory and motor areas to form an appropriate behavioral response (Harrison and Tong, 2009;Lara and Wallis, 2014;Sreenivasan et al, 2014;Pasternak et al, 2015), or alternatively, that both storage and behavioral response-related modes exist in distinct zones (Markowitz et al, 2015). The existence of a response-related mode would suggest that persistent activity during the delayed memory saccade task might be more related to the deployment of spatial attention toward the target, or the preparation of the upcoming oculomotor response.…”

“…As most synaptic connections are between neurons separated from one another by less than several hundred microns (Perin et al, 2011;Levy and Reyes, 2012), the implication is that persistent activity is associated with the presence of functional clustering. In agreement with this notion, areas such as PPC and PFC that mnemonically encode spatial location (Colby et al, 1996;Chafee and Goldman-Rakic, 1998;Rainer et al, 1998), also contain retinotopic maps (Sereno et al, 2001;Silver and Kastner, 2009;Patel et al, 2010). However, if we are to understand why stimulus-specific persistent activity generalizes to some, but not all, visual features, what is needed are studies that directly compare how different cortical areas encode different features in working memory.…”