Pulvinar inactivation disrupts selection of movement plans - PubMed (original) (raw)
Pulvinar inactivation disrupts selection of movement plans
Melanie Wilke et al. J Neurosci. 2010.
Abstract
The coordinated movement of the eyes and hands under visual guidance is an essential part of goal-directed behavior. Several cortical areas known to be involved in this process exchange projections with the dorsal aspect of the thalamic pulvinar nucleus, suggesting that this structure may play a central role in visuomotor behavior. Here, we used reversible inactivation to investigate the role of the dorsal pulvinar in the selection and execution of visually guided manual and saccadic eye movements in macaque monkeys. We found that unilateral pulvinar inactivation resulted in a spatial neglect syndrome accompanied by visuomotor deficits including optic ataxia during visually guided limb movements. Monkeys were severely disrupted in their visually guided behavior regarding space contralateral to the side of the injection in several domains, including the following: (1) target selection in both manual and oculomotor tasks, (2) limb usage in a manual retrieval task, and (3) spontaneous visual exploration. In addition, saccades into the ipsilesional field had abnormally short latencies and tended to overshoot their mark. None of the deficits could be explained by a visual field defect or primary motor deficit. These findings highlight the importance of the dorsal aspect of the pulvinar nucleus as a critical hub for spatial attention and selection of visually guided actions.
Figures
Figure 1.
Inactivation sites in the three monkeys as visualized with coinjections of gadolinium. A, Coronal anatomical MR images were collected (gray rectangle) after pulvinar inactivation. In all cases, the monkeys were fully awake and accustomed to being in the scanner. For each monkey, the center of the injection was between +3 to +5 mm in Horseley–Clark coordinates (pink rectangle). B, Coronal images depicting slices (1.75 mm thickness) around the tip of the cannula after injection, with the gadolinium appearing white. The full extents of the injections are shown in supplemental Figure 1 (available at
as supplemental material). C, Magnified view of rectangles in B shown for the three monkeys. The yellow lines correspond to thalamic landmarks derived from the anatomical monkey atlas (Saleem and Logothetis, 2007). These coronal slices were acquired between 0.5 and 1 h after infusion. Injections shown represent the maximum injection volume used in the current study (4 μl). bc, Brachium of superior colliculus; cd, caudate; dPULV, dorsal pulvinar (target structure); Gd, gadolinium; LGN, lateral geniculate nucleus; lv, lateral ventricle; r, reticular nucleus; SC, superior colliculus; vPULV, ventral pulvinar.
Figure 2.
Effects of pulvinar inactivation on reaching decisions. A, Task: treats were placed at all four tabletop positions. Monkeys sat in front of the table and retrieved the food-treats. B, Percentage trials in which an ipsilesional treat was selected first in control and inactivation sessions [_N_control = 12; _N_muscimol = 6 (3 sessions for each monkey A and C); _N_THIP = 6 (3 sessions for each monkey A and C)]. Note that, after the injection, the first reach was strongly biased toward the ipsilesional hemifield. C, Percentage ipsilesional hand usage as a function of food treat position. Whereas in control trials monkeys used both hands, inactivation resulted in nearly exclusive use of the ipsilesional hand in both animals. Error bars indicate SE across sessions. **p < 0.01.
Figure 3.
Effects of pulvinar inactivation on reaching errors and time. A, Typical reaching behavior after pulvinar inactivation. Monkey was free to choose the treat at any position and hand usage was enforced by placing a barrier in front of one hand. Note the reaching position inaccuracy when the contralesional (i.e., right) hand was used. B, Distribution of reaching errors as a function of food treat position. Shown is the proportion of corrected and uncorrected errors. Data for the two monkeys are pooled [_N_control = 12; _N_muscimol = 6 (3 sessions for each monkey A and C); _N_THIP = 6 (3 sessions for each monkey A and C)]. Note the increase of reaching errors in both sides of space when the contralesional hand was used for retrieval. C, Reaching times on trials in which monkeys were instructed to use either the ipsilesional or contralesional hand by placing a barrier in front of the opposite hand. Depicted are the reaching times as analyzed from the digital movies (one frame is 0.03 s). Note the increase in reaching time after inactivation, which was especially pronounced after muscimol injection. Error bars indicate SE across sessions. **p < 0.01.
Figure 4.
Effects of pulvinar inactivation on grasping behavior. A, Typical grasping behavior after pulvinar inactivation. Note the extended fingers and failure to shape the contralesional hand appropriately after inactivation. B, Distribution of grasping errors as a function of food treat position. Shown is the proportion of corrected and uncorrected errors. Data for the two monkeys are pooled [_N_control = 12; _N_muscimol = 6 (3 sessions for each monkey A and C); _N_THIP = 6 (3 sessions for each monkey A and C); same sessions as in Figs. 2 and 3]. Note the significant increase in grasping errors on both sides of space when the contralesional hand was used for retrieval.
Figure 5.
Spontaneous eye movements. Eye movements were recorded while monkeys were sitting with head fixed in a lit room. A, Spontaneous eye movement traces during representative sessions in monkeys A and B before injection (black) and after pulvinar inactivation (purple) with 3 μl of THIP. Each panel shows eye traces collected during a period of 60 s. Note the systematic shift of eye movements toward the ipsilesional hemifield in both monkeys A and B after pulvinar inactivation. B, Proportion of viewing time spent in different zones of the visual field for control and inactivation sessions; data pooled for monkeys A–C (_N_control = 6; _N_THIP = 6; 2 sessions for each monkey). Zones are defined as follows: ipsilesional (>5° from vertical meridian on ipsilesional side), middle (within 5° of the vertical meridian), contralesional (>5° from vertical meridian on contralesional side). Each bar in the panel on the right represents average viewing time over 4 min during each session collected 60–180 min after injection start. C, Mean eye position in control and inactivation sessions. Note the average gaze position shift toward the ipsilesional hemifield. Error bars indicate SE across sessions. **p < 0.01.
Figure 6.
Task used to evaluate saccades before and after pulvinar injections. Monkeys were trained to move their eyes to a single target, which could appear either ipsilateral or contralateral to the injection site or in both hemifields simultaneously. A trial always started with an 800 ms period of fixation in the middle of the screen, after which the targets could appear in one of four possible peripheral positions on the screen (top right, bottom right, top left, or bottom left), at eccentricities of 5° elevation and 15° azimuth. In the instructed condition, a single target appeared, to which the monkey was required to make a saccade for a reward. In the decision condition, two targets appeared simultaneously, one on the right and one on the left, and the animal was required to make a saccade to either one.
Figure 7.
Saccade performance toward instructed, single targets during control and inactivation sessions. A, Proportion of correct eye movements to targets in the ipsilesional or contralesional hemifield during control and inactivation sessions, plotted separately for the three monkeys [monkey A (_N_control = 4; _N_muscimol = 4); monkey B (_N_control = 4; _N_THIP = 4); monkey C (_N_control = 5; _N_THIP = 5)]. B, Saccade latency during the direct saccade task for monkeys A–C (see Materials and Methods). The sessions are the same as in A. On all panels, the purple lines represent data obtained after pulvinar inactivation, and the black lines represent data from control sessions. The top and bottom field data are pooled. Note that saccade latencies toward the ipsilesional field became shorter in all three monkeys after inactivation in comparison with the control data, whereas saccade latencies toward contralesional targets remained mostly unaffected. Error bars indicate SE across sessions. **p < 0.01.
Figure 8.
Effects of pulvinar inactivation on saccade decisions. A, Typical example of eye movements performed in control and inactivation sessions (monkey B). Raw eye traces (50 ms before saccade start to 50 ms after end) are overlaid from each trial for all four target positions, which were randomly interleaved during testing. The top panel depicts eye movement traces in the control session (black), whereas the bottom panel shows eye movement traces during decision trials after inactivation with THIP (purple). Note the decrease of decisions toward the contralesional targets after inactivation, even though the instructed saccades toward contralesional targets appeared normal (Fig. 7_A_). B, Proportion of eye movement decisions toward the ipsilesional field. Note the strong increase of saccades toward ipsilesional targets during inactivation sessions. The bar heights represent the mean percentage of ipsilesional target decisions over sessions. Error bars indicate SE across sessions [monkey B and C combined (monkey B (_N_control = 4; _N_THIP = 4); monkey C (_N_control = 5; _N_THIP = 5); same sessions as in Fig. 7]. **p < 0.01. C, Histograms of saccade endpoints in control and inactivation sessions in double target trials. Note the systematic shift of saccade endpoints toward the ipsilesional hemifield after inactivation. Error bars indicate SE across sessions. **p < 0.01.
References
- Acuña C, Gonzalez F, Dominguez R. Sensorimotor unit activity related to intention in the pulvinar of behaving Cebus apella monkeys. Exp Brain Res. 1983;52:411–422. - PubMed
- Acuña C, Cudeiro J, Gonzalez F, Alonso JM, Perez R. Lateral-posterior and pulvinar reaching cells—comparison with parietal area 5a: a study in behaving Macaca nemestrina monkeys. Exp Brain Res. 1990;82:158–166. - PubMed
- Andersen RA, Cui H. Intention, action planning, and decision making in parietal-frontal circuits. Neuron. 2009;63:568–583. - PubMed
- Andersen RA, Snyder LH, Li CS, Stricanne B. Coordinate transformations in the representation of spatial information. Curr Opin Neurobiol. 1993;3:171–176. - PubMed
- Arend I, Machado L, Ward R, McGrath M, Ro T, Rafal RD. The role of the human pulvinar in visual attention and action: evidence from temporal-order judgment, saccade decision, and antisaccade tasks. Prog Brain Res. 2008a;171:475–483. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources