Evidence for a Causal Contribution of Macaque Vestibular, But Not Intraparietal, Cortex to Heading Perception

Abstract

Multisensory convergence of visual and vestibular signals has been observed within a network of cortical areas involved in representing heading. Vestibular-dominant heading tuning has been found in the macaque parietoinsular vestibular cortex (PIVC) and the adjacent visual posterior sylvian (VPS) area, whereas relatively balanced visual/vestibular tuning was encountered in the ventral intraparietal (VIP) area and visual-dominant tuning was found in the dorsal medial superior temporal (MSTd) area. Although the respective functional roles of these areas remain unclear, perceptual deficits in heading discrimination following reversible chemical inactivation of area MSTd area suggested that areas with vestibular-dominant heading tuning also contribute to behavior. To explore the roles of other areas in heading perception, muscimol injections were used to reversibly inactivate either the PIVC or the VIP area bilaterally in macaques. Inactivation of the anterior PIVC increased psychophysical thresholds when heading judgments were based on either optic flow or vestibular cues, although effects were stronger for vestibular stimuli. All behavioral deficits recovered within 36 h. Visual deficits were larger following inactivation of the posterior portion of the PIVC, likely because these injections encroached upon the VPS area, which contains neurons with optic flow tuning (unlike the PIVC). In contrast, VIP inactivation led to no behavioral deficits, despite the fact that VIP neurons show much stronger choice-related activity than MSTd neurons. These results suggest that the VIP area either provides a parallel and partially redundant pathway for this task, or does not participate in heading discrimination. In contrast, the PIVC/VPS area, along with the MSTd area, make causal contributions to heading perception based on either vestibular or visual signals.

Significance statement: Multisensory vestibular and visual signals are found in multiple cortical areas, but their causal contribution to self-motion perception has been previously tested only in the dorsal medial superior temporal (MSTd) area. In these experiments, we show that inactivation of the parietoinsular vestibular cortex (PIVC) also results in causal deficits during heading discrimination for both visual and vestibular cues. In contrast, ventral intraparietal (VIP) area inactivation led to no behavioral deficits, despite the fact that VIP neurons show much stronger choice-related activity than MSTd or PIVC neurons. These results demonstrate that choice-related activity does not always imply a causal role in sensory perception.

Keywords: PIVC; VIP; heading perception; optic flow; reversible chemical inactivation; vestibular.

Figure 1.

Experimental setup, heading discrimination task, and hypothesized changes in behavioral performance following reversible inactivation. A, Using a motion platform, animals were translated forward along different heading directions in the horizontal plane. Positive heading angles correspond to rightward directions and 0° denotes straight-ahead motion. A projector mounted on the motion platform displayed images of a 3D star field and provided optic flow cues. B, Each trial began with the appearance of a small, head-centered fixation target at the center of the display. As soon as motion stimulus was completed, the fixation point disappeared and two choice targets appeared. Monkeys were required to make a saccade to one of the two targets to report their perceived heading as leftward or rightward relative to straight ahead. C, Predicted effects of inactivation on heading discrimination performance. Muscimol injection suppresses neural activity, as illustrated by a 12 s epoch of raw neural activity (inset) measured in the PIVC before and 20 min after injection of muscimol. These traces show responses to a 0.5 Hz sinusoidal lateral translation. If an area is involved in heading perception, inactivation is expected to deteriorate the precision of heading discrimination, leading to a shallower psychometric function.

Figure 2.

Anatomical localization of inactivation sites. A–D, PIVC inactivation sites in Monkeys J and Y, projected onto flat maps of cortex made with Caret software. Black and gray circles in A–D denote anterior and posterior PIVC injection sites, respectively. Each circle represents one injection site. The gray and cyan boundaries in the flat maps for Monkey J represent estimates of the regions of inactivation corresponding to pairs of muscimol injections in anterior (distance between paired injection sites: 1.96 mm for left hemisphere, 1.94 mm for right hemisphere) and posterior (distance between paired injection sites: 2.89 mm for left hemisphere, 1.79 mm for right hemisphere) PIVC, respectively. E–H, VIP inactivation sites in Monkeys J and B. Gray boundaries for Monkey J again represent estimated regions of inactivation for a pair of VIP injection sites (distance between paired injection sites: 2.71 mm for left hemisphere, 4.15 mm for right hemisphere). Each panel shows a lateral view of the 3D surface reconstruction of one hemisphere, with various functional areas denoted by colored regions [from the parcellation scheme of Lewis and Van Essen (2000a,b)].

Figure 3.

Data from an example inactivation session in which muscimol was injected into the anterior PIVC. Psychometric functions were collected at four time points: in the 2 d before muscimol injection (Pre, dashed curves and cross symbols), immediately after inactivation (0 h, orange), 12 h after inactivation (12 h, red), and 36 h after inactivation (36 h, black solid curves and open symbols). A–C, Psychometric functions are shown for the visual (A), vestibular (B), and combined (C) conditions. These data were collected following four bilateral injections of muscimol (2 in each hemisphere), with each injection having a volume of 2 μl and a concentration of 10 μg/μl (see Materials and Methods).

Figure 4.

Summary of inactivation-induced increases in heading discrimination thresholds. A, Psychophysical thresholds of Monkeys J (upper row), Y (middle row), and B (bottom row) are shown for experiments in which muscimol was injected bilaterally into the PIVC (red) or the VIP area (gold). Filled and open red symbols denote experiments involving injections into the anterior and posterior PIVC, respectively. For comparison, MSTd inactivation results are also shown for Monkey J (black; data from Gu et al., 2012). Data are shown separately for vestibular (left), visual (center), and combined (right) conditions. The abscissa in each panel marks the four different time points at which data were collected: Pre, 0 h, 12 h, or 36 h. B, Average normalized thresholds, computed by dividing the threshold at each time point by that from the preinjection (Pre) sessions. Solid and hatched red bars correspond to injections made in the anterior and posterior portions of the PIVC, respectively. Asterisks mark normalized thresholds significantly greater than unity (*p < 0.05; **p < 0.01; ***p < 0.001). Error bars: SEM. Black bars show MSTd inactivation data from three animals (replotted from Gu et al., 2012).