Intention and attention: different functional roles for LIPd and LIPv

Abstract

Establishing the circuitry underlying attentional and oculomotor control is a long-standing goal of systems neuroscience. The macaque lateral intraparietal area (LIP) has been implicated in both processes, but numerous studies have produced contradictory findings. Anatomically, LIP consists of a dorsal and ventral subdivision, but the functional importance of this division remains unclear. We injected muscimol, a GABA(A) agonist, and manganese, a magnetic resonance imaging lucent paramagnetic ion, into different portions of LIP, examined the effects of the resulting reversible inactivation on saccade planning and attention, and visualized each injection using anatomical magnetic resonance imaging. We found that dorsal LIP (LIPd) is primarily involved in oculomotor planning, whereas ventral LIP (LIPv) contributes to both attentional and oculomotor processes. Additional testing revealed that the two functions were dissociable, even in LIPv. Using our technique, we found a clear structure-function relationship that distinguishes LIPv from LIPd and found dissociable circuits for attention and eye movements in the posterior parietal cortex.

Figure 1. Behavioral tasks and example injections

a, Schematic of the memory-guided saccade and the visual search task. Saccades were directed to remembered target locations after a 1 – 1.6 s memory period. The visual search task was based on Wardak et al., : on two-thirds of trials, monkeys performed a single saccade directly to a purple target (a square) lying within a radial array of 7 purple distractors (ellipses, crosses, and triangles). On the other one-third of trials the target appeared alone, without distractors (not shown), as a control for the oculomotor effect. b + c, MRIs, reaction times (RT) and error rates from two example injections placed at different depths in the lateral bank of the IPS. Manganese mixed with muscimol resulted in a bright halo, seen here in coronal slices. Scale bars, 5 mm. The mean of saccade (grey) and search (black) RTs from each injection (solid circles) and their matched controls (hollow circles) are plotted against their corresponding error rates. Arrows show the effects of each inactivation in the RT and error rate domains. Upward and rightward directions indicate impaired behavior.

Figure 2. LIP lesion effects as a function of depth

a, Lesion-induced contralateral search error rate as a function of normalized injection depth. Inset illustrates how the full IPS depth and the lesion depth were measured for an LIPv injection from a coronal MRI slice. Filled circles represent injection sites with significant effects of either RT or errors (P < 0.025 prior to correction for the two independent comparisons). The vertical dashed line approximates the LIPd/v border. The mean LIPd effect was a change in error rate of −0.2 ± 1.4%, and the mean LIPv effect was 15.7 ± 3.4%. b, Contralateral adjusted saccade RT effect (see Supplementary Information) as a function of injection depth. Mean effects in LIPd and LIPv were 11.1 ± 1.8 ms and 10.1 ± 2.0 ms, respectively. See text for significance tests. Dotted lines are least-squares regression fits for the data, respectively. Four data points were shifted slightly to avoid overlap in a.

Figure 3. Performance of memory-guided saccades and visual search before and after LIPd and LIPv inactivations

a & b, Prevalence of significant saccadic (grey) and/or search (black) effects following LIPd and LIPv lesions. c – f, Mean adjusted saccade RT (grey) and search error rate (black) by target direction for LIPd and LIPv controls (dashed line) and injections (solid line). Large outer circles indicate 30 ms (saccade RT) or 30% (search error rate) beyond the center value. Error bars are ± 1 standard error of the difference between the control and injection values. Solid data points indicate significant effects (P < 0.05).

Figure 4. Initial eye position modulates search but not saccade effect

a, Initial eye position and all visual stimuli were displaced either 5° to the left or right for both memory-guided saccade task and visual search task. b & c, The mean effect with different eye positions on saccade RT (grey) and search error rate (black) in LIPd and LIPv. Error bars are one standard error of the mean; asterisks indicate P < 0.05.

Figure 5. Lesion overlap maps

a & b. The estimated areas of inactivation (see Supplementary Information) for all search-negative (a) and search-positive (b) injections from two fascicularis animals shown on coronal brain slices. The color palette indicates the percentage of search-negative or search-positive lesions that involved each voxel. Data are thresholded at 20%. Scale bars, 5 mm. c. The voxelwise percentage effects from a and b were subtracted and projected, without thresholding, onto the inflated cortical surface. A, anterior; P, posterior; M, medial; L, lateral; IPS, intraparietal sulcus; STS, superior temporal sulcus. Scale bar, 1 mm.

Figure 6. MRIs and search effects of control injections

Control injections were grouped into (a), large medial bank injections. (b), focal medial bank injections. (c), large LIPd + 7a injections. (d), LIPd. and (e), LIPv injections. Bars and error bars show the population effects of each injection type on search error rates in the contralateral hemifield. Error bars are one s.e.m.. Scale bars, 5 mm. Only LIPv injections produced a significant increase in search error rate. Data from the five large LIPd + 7a injections are included in the LIPd data shown in the rest of the paper.