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«Published in final edited form in: European Journal of Neuroscience. (2013) doi: dx.doi.org/10.1111/ejn.12324 Gaze direction affects linear ...»

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Under this prior, the effects of head and eye eccentricity on 〈 ̃ 〉 are indistinguishable; 〈 ̃ 〉 shifts toward both eye and head eccentricity by the same amount. This predicts that when H = -16° and E = 16° (one of the two conditions in the head eccentric paradigm), PSEs should be around 0°, which does not correspond exactly with our results (see 2nd column in Figure 7). Although failing in this point, it is in qualitative agreement with the other four conditions.

The 〈 ̃ 〉 estimates derived from the above two priors shift in the direction of eye deviation, as observed for most participants. For a few subjects, however, 〈 ̃ 〉 shifted away

from eye deviation and this would arise, for example, from a prior for zero gaze:

.

〈̃ 〉,, (10) Now the estimate 〈 ̃ 〉 shifts away from both eye and head eccentricity, as was the case for the three subjects who showed the reversed effect in the experiments with head eccentric.

The above examples illustrate that behavioral regularities, possibly other than the ones suggested here, could be behind the spurious dependencies found our results. Further experiments should investigate whether the shifts are consistent with an optimal implementation of prior information and are not simply the result of inaccuracies in the estimation process. This could be done, for example, by assessing whether the magnitude of the shifts changes when the reliability of the inertial signals is manipulated. That is, one should observe a reweighting of prior and sensory information such as has been described on a trial-by-trial basis in visuo-vestibular integration (Fetsch et al., 2009).

Head eccentricity We also found evidence of an effect of head-eccentricity on performance. In all paradigms we used the same trajectories, which were defined relative to the trunk’s straight ahead. While varying gaze does not change the sensory stimulus to the otoliths, changing head-on-trunk does. With eccentric head-on-trunk the otoliths are no longer activated along the median plane but along a deviated direction leading to a non-symmetric pattern of activation.

Systematic errors in heading direction estimation related to the deviation of the path with respect to the median plane of the head have recently been reported and reported a bias toward lateral directions (Cuturi & MacNeilage, 2013), which would predict a preponderance of rightward reports when the head is deviated to the left. In a study by Ivanenko et al. (1997) subjects with head-on-trunk deviated 45° and motion along the trunk, blind pointing at the estimated direction of motion deviated from true direction by approximately 3° in the direction of the head. Estimated trunk orientation deviated even more, about 6°, also in the direction of the head. Therefore the estimate of heading relative to the estimate of the trunk straight-ahead deviated in the direction opposite of head-on-trunk Ni, J., Tatalovic, M., Straumann, D., Olasagasti, I. (2013) Gaze direction affects linear self-motion heading discrimination in humans. European Journal of Neuroscience. doi: dx.doi.org/10.1111/ejn.12324 position. When extrapolated to our study, both studies would predict a preponderance of rightward reports when the head is deviated to the left, opposite to our findings. However, none of these studies monitored eye position, which is known to have a strong effect in localization. Moreover, one should be cautious since estimates for a given quantity will depend on the specific task.

Another difference in our experiments between eye and head eccentric conditions is that, unlike eye eccentricity, head eccentricity was not actively maintained by the participants; therefore the only available information about head-on-trunk position was that from neck proprioceptors and the knowledge of the subjects about the experimental setup. A few subjects mentioned that, when looking at the left LED, they felt that both head and trunk were facing the LED. This suggests that at least some subjects had internalized the relative positions of the objects in the platform (Figure 1) and that the known orientation of the LED in space was used as an ‘anchor’. Looking at the left LED, eye-in-head was centered, once the head-in-trunk signal has decayed the brain could interpret this situation in two ways (i) “I am looking along the trunk, therefore along the axis of the motion platform” since they know that their trunk faces the LED located straight ahead or (ii) “I am looking to an LED which I know is positioned to the left of the motion platform axis and my head feels centered on the trunk, therefore my body must be turned in the direction of the LED”. If option (ii) is favored, and this same signal is used as reference for the task, there should be an increase in rightward reports (since the reference has shifted to the left). This cannot be the main contribution in the shift of the psychometric functions since the subjects that mentioned this perception still showed a preponderance of leftward judgments. Nobody reported misperception of trunk orientation when looking at the LED located straight ahead from the trunk. In this configuration the context knowledge about LED positioning, the true trunk orientation and a decayed head signal could lead, in principle, to a perception of gaze as to the right (due to the eccentric eye position signal to the right). These cognitive effects might explain why results about the effect of head direction were more variable across subjects than those of eye direction.





Across subjects, the shifts observed in the two head-eccentric conditions were almost symmetric about zero, while one would have expected an overall leftward pattern if gaze (eye-intrunk) was the determinant factor. Here the non-balanced design of the head-eccentric paradigm, with only leftward and straight-ahead gaze, might have played a role. An initial preponderance of leftward reports might have been cancelled by an expectation of an equal number of rightward and leftward deviations that would tend to balance the total number of rightwards and leftwards reports.

These differences preclude a direct comparison of the magnitude of the head and eye eccentricity effects on the heading discrimination task.

Origin of relevant eye and head position signals Theoretically, the signals of eye position stem from two different sources: efference copies of motor commands (“outflow” or corollary discharge) and extra-ocular muscle (EOM) proprioception (“inflow”) (Donaldson, 2000; Ruskell, 1999). The outflow signal is comprised of copies of motor commands sent to the EOM, and should project to sensory pathways simultaneously (Crapse and Sommer, 2008a; 2008b). Previous research indicated that the efference copy provides a majority of the eye position information by on-line feedback (Guthrie et al., 1983; Lewis et al., 2001); while the afferent signals from the EOM may also provide complementary eye position information (Weir et al., 2000).

Ni, J., Tatalovic, M., Straumann, D., Olasagasti, I. (2013) Gaze direction affects linear self-motion heading discrimination in humans. European Journal of Neuroscience. doi: dx.doi.org/10.1111/ejn.12324 In the case of head-on-trunk, both neck proprioception and efferent copies from motor commands to move the head can provide the necessary information. In our experiments the head was not free to move, therefore neck proprioception was the only direct sensory input available. Eccentric head-on-trunk was kept continuously for at least 12 minutes, which leads to adaptation and a decreased perception of head deviation.

Conclusion We have reported for the first time an effect of eye and head direction on inertial motion direction discrimination. So far, effects of eye and head eccentricity were reported in localization tasks involving visual and/or auditory stimuli. Both source localization and heading direction estimation rely on cues from different sensory systems in different reference frames. We hypothesize that the systematic errors observed in both kinds of tasks occur because the underlying reference frames, which are referenced to eye, head or trunk, deviate from their configurations during natural behaviors. This is consistent with ideas about predictive coding and Bayesian inference in general, which propose that perception is not a pure bottom-up process, but a process incorporating contextual information and expectations (Friston, 2005). If this is the case, systematic errors with eccentric eye and/or head might be universal, while their instantiation could differ because their expected configurations might differ depending on the nature of the task.

Acknowldegments The authors would like to thank Thomas Knoepfel, Giovanni Siciliani and Timothy Bergmann for performing part of the data collection during their participation in the Human Experimental Studies course of the University of Zürich; and Marco Penner for technical help in the preparation of the experimental setup. This work was supported by Sino-Swiss Science & Technology Cooperation grant No.EG20-032010, The Swiss National Fund, the Koetser Foundation for Brain Research, Switzerland; and the Zurich Center for Integrative Human Physiology (ZIHP).

IO would like to acknowledge the support of the University of Geneva.

Abreviations

EOM: extra-ocular muscle. LED: light emitting diode. MAD: median absolute deviation. MLE:

maximum likelihood estimate. LVOR: linear vestibulo-ocular reflex. PSE: point of subjective equivalence. SEM: standard error of the mean.

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