Reply: Contributions of visual and motor signals in cervical dystonia

Sir, We appreciate the thoughtful comments from Amlang and colleagues regarding our recent viewpoint (Shaikh et al., 2016). They raise the important point that the neural integrator responsible for controlling head position relies on visual feedback in addition to feedback from the cerebellum, proprioceptors, and the basal ganglia. To address these ideas Amlang and colleagues analysed the ‘straight-ahead preference’ in subjects with cervical dystonia and compared it with that of healthy subjects. Two conditions schematizing ‘straight-ahead preference’. In Condition 1 the subject is moving straight ahead (direction of grey thick arrow), and also looking straight ahead. The target (red object) appearing on the subject’s left is projected to retinal orientation r1 in both eyes. In Condition 2 the subject is moving straight ahead (direction of grey thick arrow) but the eyes are turned to the right. The target (red object) appears straight ahead, but its image is still on the same retinal location (r1) in both eyes. The reaction time is shorter in Condition 2 compared to Condition 1 because the image of the novel target could represent an obstacle in front of the subject. The elegant experiments by Amlang and colleagues (2017) provide proof of such a principle. They found an overall increase in reaction time in subjects with cervical dystonia. The reaction time to the peripheral target location that was in line with the sagittal plane passing through the head was still less compared to a peripheral target that was eccentric compared to the head. It was unclear whether impaired visuospatial processing in cervical dystonia is the cause or consequence of these phenomena. The authors now speculate that altered visual input can affect the function of a presumed head neural integrator. We agree with this possibility as an additional mechanism for an impaired head neural integrator. Here we offer another insight on how impaired neural integration affects visuospatial processing and reaction times. Organization of the cortical coordinate transformation system, and the influence of the position of the eyes and the head neural integrator on determination of the body-fixed coordinate of the target. These results can be explained given not only the head neural integrator hypothesis, but in general as a consequence of motor uncertainty or a mismatch between the efferent motor output and the efference copy being used for transformations. There are two ways the brain receives head-on-trunk orientation. One is via an efference copy from the neural integrator and the other is from proprioceptive afference. Impairment in a head neural integrator could interfere with processing of both types of information. As a result, the position signals necessary for coordinate transformations become less faithful, possibly more noisy and consequently increase the chances of inaccuracy. To compensate for this potential for error the reaction time could be increased to give the brain more time to become more certain of the needed response. It is also possible, however, that the head neural integrator has little role in such a phenomenon and that the increase in the reaction time is merely due to extraneous ‘noise’ in proprioceptive muscle output in cervical dystonia. In such a situation, one might expect an indirect modulation of the output from the head neural integrator. Subjects with cervical dystonia often present with a jerky head tremor (Shaikh et al., 2008, 2013, 2015). These head oscillations and consequent eye oscillations (due to a tremor-induced but normal vestibulo-ocular reflex response) lead to a constantly changing head-on-trunk orientation and eye-in-orbit position. As a result, there is a discrepancy as the target image on the retina remains stable, but the head-on-trunk and eye-in-head orientations are constantly in flux. Such extraneous signals could also increase motor uncertainty and increase reaction time. Several other studies suggested that visual-spatial orientation is disrupted in cervical dystonia (Anastasopoulos et al., 1997a, b, 1998; Muller et al., 2005) showing that the perception of visual-spatial orientation is referenced to the head in normal subjects, while in cervical dystonia it is shifted to the trunk. In summary, we agree with the possibility that abnormal visuospatial processing could contribute to dysfunction of the head neural integrator. However, it is also plausible that dysfunction of the head neural integrator itself can also affect visuospatial coordinate transformations. This concept is consistent with the notion that cervical dystonia is not a disorder localized to a single brain region, but instead is a consequence of widespread impairment in a neural network responsible for sensorimotor integration. With the considerable complexity of these neural networks controlling the position of the head, disentangling the core deficit causing cervical dystonia remains a challenge. Nevertheless, the concept of a head neural integrator provides a conceptual model that may help to guide further studies of the pathophysiology of this disorder.

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