Functional imaging reveals rapid reorganization of cortical activity after parietal inactivation in monkeys

Abstract

Impairments of spatial awareness and decision making occur frequently as a consequence of parietal lesions. Here we used event-related functional MRI (fMRI) in monkeys to investigate rapid reorganization of spatial networks during reversible pharmacological inactivation of the lateral intraparietal area (LIP), which plays a role in the selection of eye movement targets. We measured fMRI activity in control and inactivation sessions while monkeys performed memory saccades to either instructed or autonomously chosen spatial locations. Inactivation caused a reduction of contralesional choices. Inactivation effects on fMRI activity were anatomically and functionally specific and mainly consisted of: (i) activity reduction in the upper bank of the superior temporal sulcus (temporal parietal occipital area) for single contralesional targets, especially in the inactivated hemisphere; and (ii) activity increase accompanying contralesional choices between bilateral targets in several frontal and parieto-temporal areas in both hemispheres. There was no overactivation for ipsilesional targets or choices in the intact hemisphere. Task-specific effects of LIP inactivation on blood oxygen level-dependent activity in the temporal parietal occipital area underline the importance of the superior temporal sulcus for spatial processing. Furthermore, our results agree only partially with the influential interhemispheric competition model of spatial neglect and suggest an additional component of interhemispheric cooperation in the compensation of neglect deficits.extinction | hemispheric imbalance | saccadic decision | recovery

Inactivation of Parietal Reach Region Affects Reaching But Not Saccade Choices in Internally Guided Decisions

“…Similar findings were also reported for saccade movements after LIP inactivation. Although these results are consistent with previous inactivation studies that used the asynchronous doubletarget paradigm (Wardak et al, 2002;Balan and Gottlieb, 2009), they differ from our findings as well as from those of previous studies (Wilke et al, , 2013 that only used the free-choice and single-target instructed tasks-i.e., reduction of contralesional choices only when both targets are simultaneously presented. These findings and the direct comparison of inactivation effects on single-target trials within and outside of the SOA task (Wardak et al, 2002) demonstrate that the behavioral context (i.e., trying to correctly report the first target, as opposed to free choice between targets associated with equal and deterministic reward in our experiments) strongly affects the pattern of inactivation-induced deficits.…”

“…However, in the inactivation sessions, the muscimol injection decreases the relative desirability of the contralesional reach options (i.e., drug injection inhibits the PRR neuronal population that encodes the desirability of the contralesional reaches), resulting in a profound choice bias toward ipsilesional targets. The motivational underpinning of inactivation-induced spatial bias is supported by our recent inactivation study of the pulvinar (which is strongly interconnected with PRR), showing that the contralesional choice deficit can be alleviated by placing a large reward in the contralesional hemifield (Wilke et al, 2013). However, the action-based theory and the notion of relative desirability in the PRR provide just a theoretical interpretation of the results and further experimental work is required to validate the hypothesis.…”

“…One way to establish whether particular regions are involved in the decision process is to temporarily perturb these regions through pharmacological inactivation and observe the effects on decision making. Studies in monkeys have shown that unilateral lateral intraparietal (LIP) area inactivation leads to a reduction of contralesional choices in oculomotor decisions (Wardak et al, 2002;Balan and Gottlieb, 2009;Wilke et al, 2012). Similar effects were found in saccade choices (Wilke et al, 2013) and in reach and grasp choices by inactivating subcortical regions, such as the pulvinar, as well as in visual search and reach target-selection tasks after inactivating the superior colliculus (McPeek and Keller, 2004;Song et al, 2011).…”

Effects of Pulvinar Inactivation on Spatial Decision-making between Equal and Asymmetric Reward Options

“…The dorsal pulvinar is reciprocally interconnected with several areas in the parietofrontal cortex such as the lateral intraparietal (LIP) area, FEF, and the dorsolateral pFC (dlPFC), where electrophysiological studies in monkeys have reported firing rate changes during cue and delay-period intervals in the context of memory saccade tasks (Takeda & Funahashi, 2002;Chafee & Goldman-Rakic, 1998;Gnadt & Andersen, 1988). Correspondingly, several studies demonstrated that lesions in these areas impair performance in memory saccade tasks (Wilke, Kagan, & Andersen, 2012;Liu, Yttri, & Snyder, 2010;Dias & Segraves, 1999;Li, Mazzoni, & Andersen, 1999;Funahashi, Bruce, & Goldman-Rakic, 1993). These studies revealed that LIP and FEF inactivation were associated with longer latencies and hypometric saccades toward contralesional positions (Dias & Segraves, 1999;Li et al, 1999), whereas dlPFC lesions did not result in longer latencies but were characterized by erroneous saccade directions (Funahashi et al, 1993).…”

Probabilistic and Single-Subject Retinotopic Maps Reveal the Topographic Organization of Face Patches in the Macaque Cortex

“…Since previous studies investigating face patches often relied on anatomically defined atlases, we have also constructed a probabilistic retinotopic atlas of monkey ventral extrastriate cortex that can be used to compare past, and to guide future, fMRI, electrophysiology (Issa and DiCarlo, 2012;Popivanov et al, 2012), and focal-perturbation experiments (Ekstrom et al, 2008;Gerits et al, 2012;Wilke et al, 2010Wilke et al, , 2012.…”