Cortical processing in vestibular navigation

C. Kennard & R.J. Leigh (Eds.) Progress in Brain Research, Vol. 171 ISSN 0079-6123 Copyright r 2008 Elsevier B.V. All rights reserved

CHAPTER 4.18

Cortical processing in vestibular navigation Barry M. Seemungal1,, Vincenzo Rizzo2, Michael A. Gresty1, John C. Rothwell2 and Adolfo M. Bronstein1 1

Department of Clinical Neuroscience, Charing Cross Hospital, Imperial College, London, UK Sobell Department of Motor Neuroscience and Movement Disorders, ION, UCL, London, UK

2

Abstract: Visual and vestibular perceptual processes are intimately related. Previous data suggest a reciprocal visual-vestibular inhibition with regard to head motion (velocity) perception with each sensory modality mediated by distinct cerebral cortical loci. The relationship between visual and vestibular perceptual processes with regard to displacement perception is unknown. In a path-reversal vestibular navigation task, we investigated the effects of early visual deprivation on vestibular perception by comparing performance and strategies employed (i.e., displacement vs. velocity matching) by a group of congenitally blind subjects to that of a sighted control group. In a second experiment in a sighted group, we attempted to disrupt firstly displacement encoding and then velocity encoding, during a path-reversal vestibular navigation task, by applying repetitive transcranial magnetic stimulation (rTMS) to the right posterior parietal cortex (PPC), vs. a left motor cortex control. Our data show that for a path-reversal vestibular navigation task, when given free choice, sighted and blind subjects can utilize both displacement- and velocity-matching strategies, and overall, both groups display equivalent performance in performing the path-reversal task. In sighted subjects, when rTMS was applied during encoding in the path-reversal task, displacement but not velocity encoding was disrupted for leftward rotations. In summary, our data suggest that early visual deprivation does not degrade the perception of vestibular signals of head velocity or of derived percepts of angular displacement. The rTMS results in the sighted group show that leftward vestibular-derived displacement perception is encoded in the right PPC, an area prominent in visuospatial perception. Thus, in contrast to current theories of vestibular head velocity perception which involve reciprocal inhibition between separate and competing visual and vestibular cortical areas, we suggest that at least for displacement perception, visual and vestibular-derived signals are encoded in a common cortical locus. Keywords: vestibular cortex; rTMS; congenital blindness; vestibular navigation; vestibular perception

Introduction

accurate locomotor turns. Sighted humans can orient in the dark using only vestibular signals (Metcalfe and Gresty, 1992; Seemungal et al., 2007). Although blind subjects can also accurately locomote in the dark (Loomis et al., 2001), it is unknown if they do so using vestibular signals. A second question is whether the neuro-anatomical substrates subserving vestibular perceptions of motion and derived angular displacement are co-localized.

During everyday locomotion, multi-sensory inputs generate perceptions of motion and position-in-space, and in the dark, these perceptions rely upon vestibular input (Glasauer et al., 2002) to enable Corresponding author. Tel.: +44(0)2088467523;

Fax: +44(0)2088467577; E-mail: [email protected] DOI: 10.1016/S0079-6123(08)00650-X

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Since vestibular and haptic signals are not isolated during walking, locomotor tasks cannot reliably inform regarding the vestibular contribution locomotor turning orientation. To answer the first question, (i.e., do the congenital blind utilize vestibular signals during angular orientation?) we used a ‘vestibular navigation’ task that isolates vestibular input (Metcalfe and Gresty, 1992; Seemungal et al., 2007). Subjects are passively rotated in yaw-axis to right or left from a fixed origin (in the dark, with white noise sound masking) on a motorized but vibrationless ‘Ba´ra´ny chair’ (‘self-rotation test’; Fig. 1A). Subjects return themselves to start using a chair-mounted joystick. A given joystick deflection provides a voltage to the chair velocity servo giving a proportionate constant chair angular velocity. In this first experiment, we did not constrain subjects’ strategies so that we could compare and contrast performance and strategy between sighted and blind subjects. Human and animal studies have demonstrated multiple cerebral cortical areas subserving vestibular processing (Guldin and Gru¨sser, 1998), although cortical areas specifically mediating vestibularderived displacement perception are unknown. In contrast, regions mediating whole-body motion perception in humans have been found via electrical cortical stimulation (ECS) in several areas including posterior superior temporal gyrus, temporoparietal junction (TMJ), and posterior parietal cortex (PPC) (Foerster, 1936; Blanke et al., 2000; Kahane et al., 2003). Functional imaging data during vertiginous stimulation also demonstrated temporal and parietal cortex activation (Bense et al., 2001; Suzuki et al., 2001; Fasold et al., 2002; Dieterich et al., 2003). The use of vertigo-inducing stimuli in functional imaging studies complicates distinguishing cortical areas subserving vestibular perception of velocity vs. derived displacement. Although use of ECS or repetitive transcranial magnetic stimulation (rTMS) to disrupt focal cortical function during an imagined self-rotation task offer advantages above correlational techniques like functional imaging (Harris and Miniussi, 2003; Zacks et al., 2003), their relevance to vestibular navigation is unclear (viz., imagined self-rotation vs. updating of one’s position during/following real rotations). Furthermore, the mental rotation literature is dis-

cordant, i.e., mental self-rotation is mediated by left PPC (viz., Zacks et al., 2003) or right TMJ (viz., Blanke et al., 2004). Vestibular perceptual studies in cortical lesion patients are complicated by the multi-focal vestibular-cortical representation (Israe¨l et al., 1995; Farrell and Robertson, 2000; Philbeck et al., 2006; Ventre-Dominey and Vallee, 2007). To overcome the drawbacks inherent to previous methodologies, we used rTMS to transiently disrupt focal cortical function during the ‘selfrotation test’ (Seemungal et al., 2008). We hypothesized that right PPC is specifically concerned with (lateralized) vestibular-derived displacement perception and tested this by disrupting right PPC function by applying rTMS during the encoding phase of the vestibular navigation task. Primary motor cortex served as a control rTMS site. Vestibular projections to motor cortical areas are important in gait and posture (Guldin and Gru¨sser, 1998); however, there is no data implicating motor cortex in spatial orientation perception. Experimental procedures Experiment 1: self-rotation test performance: sighted vs. blind groups We tested 6 congenitally blind (‘B1–B6’: mean age 38, SD 8 years) and 12 sighted subjects (‘S1–S12’: mean age 30, SD 10 years). The subjects sat on a vibration-free rotating chair in the dark with white noise sound masking via earphones (Fig. 1A). The chair could be rotated by external computer control (‘stimulus’) or the subject could actively rotate himself (‘response’) by manipulating a directionally congruent joystick, which provided a velocity demand to the servo-motor of maximum angular velocity set at 1401 for Experiment 1. In Experiment 1, chair rotational stimuli were raised cosines of 1, 2, 3, 4, 5, and 6 s duration (i.e., 1–0.33 Hz) at peak angular velocities 30, 60, 90, and 1201/s providing stimulus angles of 151–3601. The large number of stimulus-velocity profiles presented in random order obviated ‘‘counting’’ strategies in estimating travelled angle. Subjects were instructed to return actively to the start position as accurately as possible, by moving in the opposite direction to the stimulus movement. The task can be performed

341

A

Apparatus

B

Displacement - matching strategy Inertial stimulus

Rightward 20 deg/s

2 sec

Memory

20 Leftward

Encoding Inertial response

Retrieval

TMS

C

Velocity - matching strategy

Inertial stimulus

Memory Encoding Inertial response TMS

Retrieval

Fig. 1. Apparatus and representative angular chair velocity recordings. (A) Top left panel: The motorized rotating chair with joystick control and headphones with white-noise masking. Top right panel: TMS coil mounting. (B) Representative chair angular velocity trace — rightward stimulus rotation (upward on trace) of ‘raised cosine’ waveform followed by leftward rotation response of trapezoidal shape. Trapezoidal responses signify displacement-matching responses (required in Experiment 2). (C) Representative velocity-matching trace showing similarity in shape between stimulus and response velocity profiles. Velocity matching was required in Experiment 3.

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by different strategies of the type shown for Experiment 2 (Fig. 1B: displacement-matching) or Experiment 3 (Fig. 1C: velocity-matching). In Experiment 1, subject strategy (unlike that for Experiments 2 and 3) was not constrained; subjects benefited from 15 min of free practice and a practice experiment without vision or audition. Experiment 2: right PPC vs. left motor cortex rTMS during displacement matching We tested five right-handed normal subjects (average age 34 years, range 25–50 years; four male) who gave their written consent. Subject strategy was constrained to a displacement-matching strategy (Fig. 1B) by explicitly telling subjects to return to the start position by imagining the stimulus angle travelled but also by limiting the maximum joystick-driven velocity to 601/s (which precluded a velocity-matching strategy). Stimulus rotations were identical to Experiment 1 except that only rotations of 1, 2, and 3 s duration were used to avoid prolonged periods of rTMS. Apart from the constraints on subject strategy and rotation durations, conditions were identical to Experiment 1, including a period of free practice and a practice experiment without TMS. Experiment 3: right PPC vs. left motor cortex rTMS during velocity matching The same five subjects from Experiment 2 were told to explicitly recapitulate the kinetics of inertial stimuli (Fig. 1C), and a peak joystick-driven chair velocity of 1401/s enabled this strategy. We have shown equivalent spatial performance when subjects reproduce displacement or kinetic parameters in the self-rotation test (Seemungal et al., 2007). Apart from the required strategy, conditions were identical to those in Experiment 2. TMS rTMS was applied during the encoding phase of the vestibular navigation task as shown in Fig. 1B (Experiment 2) and 1C (Experiment 3). The order in which subjects received parietal vs. motor cortex

stimulation was alternated between subjects. The handle of a figure-of-eight coil (outer windings 9 cm) was fixed to the chair via an adjustable mount while the coil was located over the scalp stimulation site. The subject’s head was stabilized as in Fig. 1A. The best position for stimulating the motor representation of the first dorsal interroseous in the left motor cortex was located by observing the amplitude of TMS-induced muscle contractions while subjects were at rest. The motor threshold intensity at this optimal site was defined as the intensity that produced a visible hand movement in three or more trials out of six. The TMS parietal scalp sites (P3 and P4) were located according to the 10–20 international EEG electrode system (Klem et al., 1999). P3 and P4 are known to overly the parietal cortex close to the intraparietal sulcus (Hilgetag et al., 2001). We stimulated motor and parietal cortex at 10% below motor threshold at 10 Hz. The number of TMS pulses applied per rotation duration was as follows: 1 s: 4 pulses, 2 s: 8 pulses, 3 s: 12 pulses. Data analysis Experiment 1 Displacement performance Quantitative analysis of displacement performance (for group and individuals) was obtained by linear regression between response and stimulus displacements. Regression slopes of sighted and blind groups’ displacement performances were compared using a 2-tailed t-test, and correlation coefficients were compared using Fisher’s r-to-z transformation. Navigational strategy Multiple regression analysis was used to quantify subjects’ strategy in vestibular navigational task by identifying the stimulus parameters that most predicted response displacement. Experiments 2 and 3 Performance was ascertained for each angular response via absolute percentage error. Displacement

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performance was analysed via repeated-measures two-way ANOVA with factors cortical locus (motor vs. parietal) and inertial stimulus direction (rightward vs. leftward). Absolute percentage errors made in peak velocity reproduction in Experiment 3 were similarly analysed. Responses to 151 stimuli were excluded from all analyses, since a subanalysis of previous data (Seemungal et al., 2007) showed that this was the only stimulus angle which elicited a significantly different absolute percentage error of angular response (larger) compared to the average response for all stimulus angles combined (119.6% vs. 43.2%; P=0.0007; t-test).

Results Experiment 1 Self-rotation test: Sighted subjects’ displacement performance and strategy Sighted subjects were highly consistent in reproducing the angular displacement with a cumulative regression analysis between response (R) and stimulus (S) displacements of the non-averaged data (n=561) yielding R=0.76S+311 and an r2

400

Experiment 1: Self-rotation test: Sighted and Blind group performance

Response (deg)

300

200

100

Sighted Blind

0

100

200

300

400

Stimulus (deg) Fig. 2. Experiment 1 results: Group performance in the selfrotation task (71 standard error).

of 0.80. Figure 2 shows the averaged angular responses for each stimulus angle for the sighted group. Individual performances (Table 1), ‘Displacement performance’, for subjects S1–S12 were similarly consistent with r2 for linear regressions between response and stimulus displacements range 0.75–0.94 (Po0.0001 for all). Individuals’ strategy is summarized in Table 1, right-hand side, ‘Predictors of response angle,’ for subjects S1–S12. Self-rotation test: Blind subjects’ displacement performance and strategy The Blind group’s self-rotation test performance (R=0.74S+171; r2=0.77; n=287) was not significantly different (PW0.05) from the sighted for slope (t-test) and r2 values (Fisher’s r transformation) for their respective regressions of the nonaveraged data (Fig. 2). Blind individuals’ strategy (Table 1) was predominantly displacement matching, although one subject (B2) utilized a predominantly velocity-matching strategy. Experiment 2 Angular displacement encoding: right PPC vs. left motor cortex rTMS Right parietal rTMS (Fig. 3A) elicited an asymmetrical displacement response (2-tailed, paired t-test: Po0.008). Control motor cortex rTMS elicited a symmetrical displacement response (t-test: P=0.56). A repeated-measures ANOVA with factors, cortical locus of rTMS (parietal vs. motor), and inertial stimulus direction (right vs. leftward) showed no main effect of inertial stimulus direction [F(1,109)= 2.35; P=0.13] or cortical locus of rTMS [F(1,109)= 0.452; P=0.50] but there was a significant interaction between cortical location of rTMS and stimulus direction [F(1,109)=5.541; P=0.020]. The observed significant interaction implies that right PPC encodes leftward vestibular-derived displacement perception. There were no significant effects of rTMS on response percentage error of peak angular velocity for both rTMS locations (repeated-measures ANOVA).

344 Table 1. Individual performance and strategy during ‘self-rotation’ test Subject (S=sighted; B=blind)

Displacement performance (linear regression response vs. stimulus angle)

Predictors of response angle via multi-regression fit (response angle vs. stimulus angle, velocity, time, acceleration)

Linear regression

Multi-regression fit

2

S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 B1 B2 B3 B4 B5 B6

2

Angle

Velocity

Time

Acceleration

b

b

b

r

B

N

r

b

0.90 0.83 0.92 0.82 0.80 0.94 0.89 0.74 0.90 0.79 0.75 0.90 0.73 0.74 0.71 0.88 0.61 0.93

1.0 0.76 0.83 0.61 0.63 1.0 0.83 0.78 0.74 0.55 0.58 0.74 0.90 0.63 0.47 0.81 0.71 1.0

48 48 48 48 47 43 48 48 47 48 48 48 48 48 47 48 48 48

0.81 0.88 0.93 0.83 0.82 0.94 0.90 0.78 0.90 0.81 0.84 0.90 0.74 0.79 0.73 0.90 0.63 0.95

0.57

0.34 0.38

0.72 0.29 0.40

0.68 0.49 0.70 1.00 0.69 0.60 0.78

0.39

0.23 0.36 0.48 0.71

0.32

0.73

0.44

0.39

0.30

0.86 1.2 

0.68 

1.2

0.26

Linear and multiple regressions for individual data, viz., correlation coefficients r2, and slopes, both standardized (b) and unstandardized (B) (nonsignificant values, i.e., PW0.05, are omitted). Strategy, which was unconstrained, is shown by the reported b values under the respective columns, e.g., a spatial strategy was signified by high b values in the ‘Angle’ column as in S6. Notes: B3 and B5 respective strategies during the self-rotation test were best described as displacement matching since, although multiple regression analyses did not yield any significant b values, those for ‘Angle’ approached significance, i.e., Po0.08 (denoted by ).

A

Experiment 2 - Displacement matching

B

Experiment 3 - Kinetic matching

P < 0.008 P > 0.05 for all

20

30

20 left rotation

right rotation

left rotation

10

right rotation

left rotation

right rotation

left rotation

% error angular response

30

10

4 40

P = 0.56

right rotation

% error angular response

40

0

Parietal cortex rTMS

Motor cortex rTMS

Parietal cortex Motor cortex rTMS rTMS

Fig. 3. The main results for Experiments 2 and 3. (A) Experiment 2: Absolute percentage error of response displacement for rightward or leftward inertial stimuli for displacement-matching task. (B) Experiment 3: Absolute percentage error of response displacement divided according to rightward or leftward inertial stimulus direction for velocity-matching task.

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Experiment 3 Angular velocity encoding: right PPC vs. left motor cortex rTMS Repetitive TMS had no effect on displacement (Fig. 3B) or velocity response symmetry (paired t-tests and ANOVA: PW0.05 for all).

Discussion Our findings indicate that angular path reversal under vestibular guidance can be successfully performed via two main strategies, i.e., displacement or velocity matching. The equivalence in performance between blind and sighted groups combined with the fact that blind subjects used either strategy in task performance indicate that the perception of raw and derived vestibular signals are entirely independent of visual mechanisms. Interestingly however, previous data has shown that blind subjects as a group appear to be less able than the sighted at inferential vestibular navigation, i.e., navigation tasks requiring mental manipulation, as opposed to a simple reproduction of the stimulus angle, for their successful completion (Seemungal et al., 2007). We found that when sighted subjects employed a displacement-matching strategy during the selfrotation task, rTMS to the right PPC disrupted encoding of vestibular-derived displacement perception. In contrast, when subjects employed a velocity-matching strategy, right parietal rTMS had no effect on encoding displacement or velocity perception. Although the use of rTMS to disrupt vestibular perception is novel, rTMS at parietal sites P3 and P4, at similar TMS intensities (10% below motor threshold), has been shown to interfere with sensory perception (Oliveri et al., 2000), mental rotation (Bestmann et al., 2002), and working memory (Mottaghy et al., 2002). The main human vestibular cortex is thought to be TMJ and contiguous posterior superior temporal gyrus (Foerster, 1936; Penfield, 1957; Friberg et al., 1985; Israe¨l et al., 1995; Blanke et al., 2000, 2004; Bense et al., 2001; Suzuki et al., 2001; Fasold et al., 2002; Dieterich et al., 2003; Kahane et al.,

2003). Concomitantly, animal data show primarily a head-velocity-processing role in this region (Guldin and Gru¨sser, 1998). Vestibular percepts of self-motion have also been demonstrated by electrical cortical activation in the area to that which we applied rTMS; that is, in close proximity to the intraparietal sulcus (Foerster, 1936; Penfield, 1957; Blanke et al., 2000) although, in support of our findings that this area primarily mediates vestibular-derived displacement perception, Snyder et al. (1998) recorded vestibular-derived position signals in primates at this locus. Lesion studies, although inconsistent in result, support the finding of a right PPC encoding of vestibular-derived displacement encoding (Israe¨l et al., 1995; Farrell and Robertson, 2000; Philbeck et al., 2006; Ventre-Dominey and Vallee, 2007). One problem with lesion studies, however, is that deficits in reference frame transformations rather than deficits in perceptual encoding may complicate data interpretation; for example, different reference frames and neuronal substrates are engaged during reaching under visual versus proprioceptive guidance (Battaglia-Mayer and Caminiti, 2002). Similarly, transformation of vestibular cues into other reference frames required in previous lesion studies (e.g., manual pointing, Philbeck et al., 2006; or saccades, Ventre-Dominey and Vallee, 2007) contrast with our use of vestibular guidance in both stimulus and response phases. Previous human data suggest that the posterior parietal cortex mediates egocentric visuo-spatial orientation (Spiers and Maguire, 2007). This data combined with our own findings suggests that the PPC may represent a common locus mediating egocentric spatial orientation perception for both visual and vestibular input. This contrasts with theories of visual and vestibular velocity perception that invoke a reciprocal inhibition between visual and vestibular cortical areas (Brandt et al., 2002). In summary, the right PPC encodes vestibularderived signals of leftward angular displacement but not angular velocity. Although visual experience does not affect vestibular perception, in sighted subjects, the PPC may represent a common locus for the convergence of visual and vestibular position signals in providing an accurate percept of egocentric spatial orientation.

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