Florian Ostendorf

Human thalamus contributes to perceptual stability across eye movements

We continuously move our eyes when we inspect a visual scene. Although this leads to a rapid succession of discontinuous and fragmented retinal snapshots, we perceive the world as stable and coherent. Neural mechanisms underlying visual stability may depend on internal monitoring of planned or ongoing eye movements. In the macaque brain, a pathway for the transmission of such signals has been identified that is relayed by central thalamic nuclei. Here, we studied a possible role of this pathway for perceptual stability in a patient with a selective lesion affecting homologous regions of the human thalamus. Compared with controls, the patient exhibited a unilateral deficit in monitoring his eye movements. This deficit was manifest by a systematic inaccuracy both in successive eye movements and in judging the locations of visual stimuli. In addition, perceptual consequences of oculomotor targeting errors were erroneously attributed to external stimulus changes. These findings show that the human brain draws on transthalamic monitoring signals to bridge the perceptual discontinuities generated by our eye movements.

Perisaccadic Compression Correlates with Saccadic Peak Velocity: Differential Association of Eye Movement Dynamics with Perceptual Mislocalization Patterns

Objects flashed around the onset of a saccadic eye movement are grossly mislocalized. Perisaccadic mislocalization has been related to a spatiotemporal misalignment of an extraretinal eye position signal with the corresponding saccade. Two phenomena have been observed: a systematic shift of perceived positions in saccade direction and an additional compression toward the saccade target. At present, it is unclear whether these two components of mislocalization are mediated by distinct mechanisms and how extraretinal signals may contribute to either of them. Moreover, the pattern and strength of perisaccadic mislocalization varies considerably across studies and even between subjects tested under identical conditions. Here, we investigated whether interindividual differences in saccade parameters are related to differences in mislocalization. We found that the individual strength of perceptual compression selectively correlates with the peak velocity of corresponding saccades. Other saccade parameters did not correlate with compression. No correlation was found between the shift component of perisaccadic mislocalization and any saccade parameter. This dissociation suggests that shift and compression components are, at least partially, mediated by distinct mechanisms. Because neuronal activity in the superior colliculus and downstream oculomotor areas has been shown to correlate with saccadic peak velocity, our findings support the notion that a reafferent extraretinal signal associated with saccadic motor commands may contribute to perisaccadic compression of perceived positions.

Reorganization of associative memory in humans with long-standing hippocampal damage

Conflicting theories have been advanced to explain why hippocampal lesions affect distinct memory domains and spare others. Recent findings in monkeys suggest that lesion-induced plasticity may contribute to the seeming preservation of some of these domains. We tested this hypothesis by investigating visuo-spatial associative memory in two patient groups with similar surgical lesions to the right medial temporal lobe, but different preoperative disease courses (benign brain tumours, mean: 1.8 +/- 0.6 years, n = 5, age: 28.2 +/- 4.0 years; hippocampal sclerosis, mean: 16.8 +/- 1.9 years, n = 9, age: 38.9 +/- 4.1 years). Compared to controls (n = 14), tumour patients showed a significant delay-dependent deficit in memory of colour-location associations. No such deficit was observed in hippocampal sclerosis patients, which appeared to benefit from a compensatory mechanism that was inefficient in tumour patients. These results indicate that long-standing hippocampal damage can yield significant functional reorganization of the neural substrate underlying memory in the human brain. We suppose that this process accounts for some of the discrepancies between results from previous lesion studies of the human medial temporal lobe.

A role of the human thalamus in predicting the perceptual consequences of eye movements

Internal monitoring of oculomotor commands may help to anticipate and keep track of changes in perceptual input imposed by our eye movements. Neurophysiological studies in non-human primates identified corollary discharge (CD) signals of oculomotor commands that are conveyed via thalamus to frontal cortices. We tested whether disruption of these monitoring pathways on the thalamic level impairs the perceptual matching of visual input before and after an eye movement in human subjects. Fourteen patients with focal thalamic stroke and 20 healthy control subjects performed a task requiring a perceptual judgment across eye movements. Subjects reported the apparent displacement of a target cue that jumped unpredictably in sync with a saccadic eye movement. In a critical condition of this task, six patients exhibited clearly asymmetric perceptual performance for rightward vs. leftward saccade direction. Furthermore, perceptual judgments in seven patients systematically depended on oculomotor targeting errors, with self-generated targeting errors erroneously attributed to external stimulus jumps. Voxel-based lesion-symptom mapping identified an area in right central thalamus as critical for the perceptual matching of visual space across eye movements. Our findings suggest that trans-thalamic CD transmission decisively contributes to a correct prediction of the perceptual consequences of oculomotor actions.

A dysexecutive syndrome of the medial thalamus

Thalamic stroke is associated with neurological and cognitive sequelae. Resulting neuropsychological deficits vary with the vascular territory involved. Whereas sensory, motor and memory deficits following thalamic stroke are comparatively well characterized, the exact relationship between executive dysfunction and thalamic damage remains more ambiguous. To assess the pattern of executive-cognitive deficits following thalamic stroke and its possible association with distinct thalamic nuclei, 19 patients with focal thalamic lesions were examined with high-resolution structural imaging and neuropsychological testing. Twenty healthy individuals served as controls. Patient MRIs were co-registered to an atlas of the human thalamus. Lesion overlap and subtraction analyses were used for lesion-to-symptom mapping. In eight patients (42.1%), neuropsychological assessment demonstrated a disproportionate deficit in the Wisconsin Card Sorting Test (WCST), while other executive and memory functions were much less affected. Subtraction analysis revealed an area in the left medial thalamus, mainly consisting of the centromedian and parafascicular nuclei (CM-Pf complex) that was damaged in these patients and spared in patients with normal WCST performance. Thus, damage to the CM-Pf complex may yield a distinct dysexecutive syndrome in which deficient maintenance and shifting between cognitive sets predominates. We hypothesize that the CM-Pf complex may contribute to maintenance and shifting of cognitive sets by virtue of its dense connections with the striatum. The pattern of executive dysfunction following thalamic stroke may vary considerably with lesion location.

Cross-modal effects of value on perceptual acuity and stimulus encoding

Significance Reward-predicting signals could be acquired through any of our different sensory modalities, but should be used by other senses to achieve fast and accurate behavior. How reward information is communicated across different sensory modalities is unknown. We demonstrate that sounds associated with high rewards increase the sensitivity of vision, even when sounds and their reward associations are task-irrelevant. Multivariate analysis of the simultaneously acquired functional MRI data revealed that high-reward sounds increased the accuracy of stimulus representation in the visual cortex. Multisensory regions of the temporal cortex were modulated by sound values, and the strength of this modulation was correlated with the change in visual acuity. Our results demonstrate a value-driven cross-modal interaction that affects early stages of sensory processing and involves multisensory areas. Cross-modal interactions are very common in perception. An important feature of many perceptual stimuli is their reward-predicting properties, the utilization of which is essential for adaptive behavior. What is unknown is whether reward associations in one sensory modality influence perception of stimuli in another modality. Here we show that auditory stimuli with high-reward associations increase the sensitivity of visual perception, even when sounds and reward associations are both irrelevant for the visual task. This increased sensitivity correlates with a change in stimulus representation in the visual cortex, indexed by increased multivariate decoding accuracy in simultaneously acquired functional MRI data. Univariate analysis showed that reward associations modulated responses in regions associated with multisensory processing in which the strength of modulation was a better predictor of the magnitude of the behavioral effect than the modulation in classical reward regions. Our findings demonstrate a value-driven cross-modal interaction that affects perception and stimulus encoding, with a resemblance to well-described modulatory effects of attention. We suggest that multisensory processing areas may mediate the transfer of value signals across senses.

Saccades to spatially extended targets: the role of eccentricity

Size and eccentricity of visual targets are known to modulate saccade parameters. Here we asked for a possible interaction between these target properties. We investigated latency and amplitude of saccades to targets of varying diameter presented at various eccentricities in the visual field. Effects of target size on saccadic eye movements highly depended on eccentricity of saccade targets. For large saccade targets, latencies increased and mean amplitudes decreased mainly at parafoveal eccentricities. By contrast, scatter of saccade amplitudes increased nearly linearly with target size and eccentricity. These effects are consistent with the known functional anatomy of the superior colliculus. Size- and eccentricity-related changes in saccade parameters may depend on distinct subpopulations of collicular neurons.

Impairment of saccade adaptation in a patient with a focal thalamic lesion

The frequent jumps of the eyeballs-called saccades-imply the need for a constant correction of motor errors. If systematic errors are detected in saccade landing, the saccade amplitude adapts to compensate for the error. In the laboratory, saccade adaptation can be studied by displacing the saccade target. Functional selectivity of adaptation for different saccade types suggests that adaptation occurs at multiple sites in the oculomotor system. Saccade motor learning might be the result of a comparison between a prediction of the saccade landing position and its actual postsaccadic location. To investigate whether a thalamic feedback pathway might carry such a prediction signal, we studied a patient with a lesion in the posterior ventrolateral thalamic nucleus. Saccade adaptation was tested for reactive saccades, which are performed to suddenly appearing targets, and for scanning saccades, which are performed to stationary targets. For reactive saccades, we found a clear impairment in adaptation retention ipsilateral to the lesioned side and a larger-than-normal adaptation on the contralesional side. For scanning saccades, adaptation was intact on both sides and not different from the control group. Our results provide the first lesion evidence that adaptation of reactive and scanning saccades relies on distinct feedback pathways from cerebellum to cortex. They further demonstrate that saccade adaptation in humans is not restricted to the cerebellum but also involves cortical areas. The paradoxically strong adaptation for outward target steps can be explained by stronger reliance on visual targeting errors when prediction error signaling is impaired.

Integration of Retinal and Extraretinal Information across Eye Movements

Visual perception is burdened with a highly discontinuous input stream arising from saccadic eye movements. For successful integration into a coherent representation, the visuomotor system needs to deal with these self-induced perceptual changes and distinguish them from external motion. Forward models are one way to solve this problem where the brain uses internal monitoring signals associated with oculomotor commands to predict the visual consequences of corresponding eye movements during active exploration. Visual scenes typically contain a rich structure of spatial relational information, providing additional cues that may help disambiguate self-induced from external changes of perceptual input. We reasoned that a weighted integration of these two inherently noisy sources of information should lead to better perceptual estimates. Volunteer subjects performed a simple perceptual decision on the apparent displacement of a visual target, jumping unpredictably in sync with a saccadic eye movement. In a critical test condition, the target was presented together with a flanker object, where perceptual decisions could take into account the spatial distance between target and flanker object. Here, precision was better compared to control conditions in which target displacements could only be estimated from either extraretinal or visual relational information alone. Our findings suggest that under natural conditions, integration of visual space across eye movements is based upon close to optimal integration of both retinal and extraretinal pieces of information.