Thomas Haarmeier

Alpha oscillations correlate with the successful inhibition of unattended stimuli.

Because the human visual system is continually being bombarded with inputs, it is necessary to have effective mechanisms for filtering out irrelevant information. This is partly achieved by the allocation of attention, allowing the visual system to process relevant input while blocking out irrelevant input. What is the physiological substrate of attentional allocation? It has been proposed that alpha activity reflects functional inhibition. Here we asked if inhibition by alpha oscillations has behavioral consequences for suppressing the perception of unattended input. To this end, we investigated the influence of alpha activity on motion processing in two attentional conditions using magneto-encephalography. The visual stimuli used consisted of two random-dot kinematograms presented simultaneously to the left and right visual hemifields. Subjects were cued to covertly attend the left or right kinematogram. After 1.5 sec, a second cue tested whether subjects could report the direction of coherent motion in the attended (80%) or unattended hemifield (20%). Occipital alpha power was higher contralateral to the unattended side than to the attended side, thus suggesting inhibition of the unattended hemifield. Our key finding is that this alpha lateralization in the 20% invalidly cued trials did correlate with the perception of motion direction: Subjects with pronounced alpha lateralization were worse at detecting motion direction in the unattended hemifield. In contrast, lateralization did not correlate with visual discrimination in the attended visual hemifield. Our findings emphasize the suppressive nature of alpha oscillations and suggest that processing of inputs outside the field of attention is weakened by means of increased alpha activity.

Disorders of Agency in Schizophrenia Correlate with an Inability to Compensate for the Sensory Consequences of Actions

Psychopathological symptoms in schizophrenia patients suggest that the concept of self might be disturbed in these individuals [1]. Delusions of influence make them feel that someone else is guiding their actions, and certain kinds of their hallucinations seem to be misinterpretations of their own inner voice as an external voice, the common denominator being that self-produced information is perceived as if coming from outside. If this interpretation were correct, we might expect that schizophrenia patients might also attribute the sensory consequences of their own eye movements to the environment rather than to themselves, challenging the percept of a stable world. Indeed, this seems to be the case because we found a clear correlation between the strength of delusions of influence and the ability of schizophrenia patients to cancel out such self-induced retinal information in motion perception. This correlation reflects direct experimental evidence supporting the view that delusions of influence in schizophrenia might be due to a specific deficit in the perceptual compensation of the sensory consequences of ones own actions [1, 2, 3, 4, 5 and 6].

Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease

The term short‐term saccadic adaptation (STSA) captures our ability to unconsciously move the endpoint of a saccade to the final position of a visual target that has jumped to a new location during the saccade. STSA depends on the integrity of the cerebellar vermis. We tested the hypothesis that STSA reflects the working of a cerebellar mechanism needed to avoid ‘fatigue’, a gradual drop in saccade amplitude during a long series of stereotypic saccades. To this end we compared the kinematics of saccades of 14 patients suffering from different forms of cerebellar disease with those of controls in two tests of STSA and a test of saccadic resilience. Controls showed an increase in saccade amplitude (SA) for outward adaptation, prompted by outward target shifts, due to an increase in saccade duration (SD) in the face of constant peak velocity (PV). The decrease in SA due to inward adaptation was, contrariwise, accompanied by a drop in PV and SD. Whereas patients with intact vermis did not differ from controls, those with vermal pathology lacked outward adaptation: SD remained constant, as did SA and PV. In contrast, vermal patients demonstrated a significant decrease in SA, paralleled by a decrease in PV but mostly unaltered SD in the inward adaptation experiment as well as in the resilience test. These findings support the notion that inward adaptation is at least partially based on uncompensated fatigue. On the other hand, outward adaptation reflects an active mechanism for the compensation of fatigue, residing in the cerebellum.

False perception of motion in a patient who cannot compensate for eye movements

We are usually unaware of the motion of an image across our retina that results from our own movement. For instance, during slow-tracking eye movements we do not mistake the shift of the image projected onto the retina for motion of the world around us, but instead perceive a stable world. Following early suggestions by von Helmholtz, it is commonly believed that this spatial stability is achieved by subtracting the retinal motion signal from an internal reference signal, such as a copy of the movement command (efference copy). Object motion is perceived only if the two differ. Although this concept is widely accepted, its anatomical underpinning remains unknown. Here we describe the case of a patient with bilateral extrastriate cortex lesions, suffering from false perception of motion due to an inability to take eye movements into account when faced with self-induced retinal image slip. This is indicated by the fact that during smooth-pursuit eye movements, he perceives motion of the stationary world at a velocity that corresponds to the velocity of his eye movement; that is, he perceives the raw retinal image slip uncorrected for his own eye movements. We suspect that this deficiency reflects damage of a distinct parieto-occipital region that disentangles self-induced and externally induced visual motion by comparing retinal signals with a reference signal encoding eye movements and possibly ego-motion in general.

Optimizing Visual Motion Perception during Eye Movements

We usually perceive a stationary, stable world and we are able to correctly estimate the direction of heading from optic flow despite coherent visual motion induced by eye movements. This astonishing example of perceptual invariance results from a comparison of visual information with internal reference signals predicting the visual consequences of an eye movement. Here we demonstrate that the reference signal predicting the consequences of smooth-pursuit eye movements is continuously calibrated on the basis of direction-selective interactions between the pursuit motor command and the rotational flow induced by the eye movement, thereby minimizing imperfections of the reference signal and guaranteeing an ecologically optimal interpretation of visual motion.

The attentive cerebellum — myth or reality?

Based on the discovery of significant cerebellar projections into associative cortices and the observation of cerebellar abnormalities in autistic children, the concept has been put forward that the cerebellum might contribute to cognitive functions including attention. Specifically, a deficit analogous to motor dysmetria has been envisaged as a consequence of cerebellar damage-the ‘dysmetria of attention’. This paper provides a review of patient studies and imaging studies which have been performed so far in order to test this concept. Although several sudies report on attention deficits of patients with cerebellar damage, a closer look at the specific paradigms used reveals that disturbances have only been observed consistently for tasks involving significant oculomotor, motor, and/or working memory demands. Likewise, cerebellar activations in imaging studies on attention seem to reflect oculomotor or other motor behavior rather than true involvement in attention. Both attempts have failed so far to consistently reveal cerebellar involvement in attention when confounding influences were controlled. We, therefore, conclude that the concept of attentional dysmetria as a consequence of cerebellar damage is not adequately supported.

Cross-frequency coupling of brain oscillations indicates the success in visual motion discrimination

Cortical activity such as recorded by EEG or MEG is characterized by ongoing rhythms that encompass a wide range of temporal and spatial scales. Recent studies have suggested an oscillatory hierarchy with faster oscillations being locked to preferred phases of underlying slower waves, a functional principle applied up to the level of action potential generation. We here tested the idea that amplitude-phase coupling between frequencies might serve the detection of weak sensory signals. To this end we recorded neuromagnetic responses during a motion discrimination task using near-threshold stimuli. Amplitude modulation of occipital high-frequency oscillations in the gamma range (63+/-5 Hz) was phase locked to a slow-frequency oscillation in the delta band (1-5 Hz). Most importantly, the strength of gamma amplitude modulation reflected the success in visual discrimination. This correlation provides evidence for the hypothesis that coupling between low- and high-frequency brain oscillations subserves signal detection.

Cerebrocerebellar Circuits for the Perceptual Cancellation of Eye-movement-induced Retinal Image Motion

Despite smooth pursuit eye movements, we are unaware of resultant retinal image motion. This example of perceptual invariance is achieved by comparing retinal image slip with an internal reference signal predicting the sensory consequences of the eye movement. This prediction can be manipulated experimentally, allowing one to vary the amount of self-induced image motion for which the reference signal compensates and, accordingly, the resulting percept of motion. Here we were able to map regions in CRUS I within the lateral cerebellar hemispheres that exhibited a significant correlation between functional magnetic resonance imaging signal amplitudes and the amount of motion predicted by the reference signal. The fact that these cerebellar regions were found to be functionally coupled with the left parieto-insular cortex and the supplementary eye fields points to these cortical areas as the sites of interaction between predicted and experienced sensory events, ultimately giving rise to the perception of a stable world despite self-induced retinal motion.

Modification of the filehne illusion by conditioning visual stimuli

During smooth pursuit eye movements made across a stationary background an illusory motion of the background is perceived (Filehne illusion). The present study was undertaken in order to test if the Filehne illusion can be influenced by information unrelated to the retinal image slip prevailing and to the eye movement being executed. The Filehne illusion was measured in eight subjects by determining the amount of external background motion required to compensate for the illusory background motion induced by 12 deg/sec rightward smooth pursuit. Using a two-alternative forced-choice method, test trials, which yielded the estimate of the Filehne illusion, were randomly interleaved with conditioning trials, in which high retinal image slip was created by background stimuli moving at a constant horizontal velocity. There was a highly reproducible monotic relationship between the size and direction of the Filehne illusion and the velocity of the background stimulus in the conditioning trials with the following extremes: large Filehne illusions with illusory motion to the right occurred for conditioning stimuli moving to the left, i.e. opposite to the direction of eye movement in the test trials, while conversely, conditioning stimuli moving to the right yielded Filehne illusions close to zero. Additional controls suggest that passive motion aftereffects are unlikely to account for the modulation of the Filehne illusion by the conditioning stimulus. We hypothesize that this modification might reflect the dynamic character of the networks elaborating spatial constancy.

An Electrophysiological Correlate of Visual Motion Awareness in Man

It is usually held that perceptual spatial stability, despite smooth pursuit eye movements, is accomplished by comparing a signal reflecting retinal image slip with an internal reference signal, encoding the eye movement. The important consequence of this concept is that our subjective percept of visual motion reflects the outcome of this comparison rather than retinal image slip. In an attempt to localize the cortical networks underlying this comparison and therefore our subjective percept of visual motion, we exploited an imperfection inherent in it, which results in a movement illusion. If smooth pursuit is carried out across a stationary background, we perceive a tiny degree of illusionary background motion (Filehne illusion, or FI), rather than experiencing the ecologically optimal percept of stationarity. We have recently shown that this illusion can be modified substantially and predictably under laboratory conditions by visual motion unrelated to the eye movement. By making use of this finding, we were able to compare cortical potentials evoked by pursuit-induced retinal image slip under two conditions, which differed perceptually, while being identical physically. This approach allowed us to discern a pair of potentials, a parieto-occipital negativity (N300) followed by a frontal positivity (P300), whose amplitudes were solely determined by the subjective perception of visual motion irrespective of the physical attributes of the situation. This finding strongly suggests that subjective awareness of visual motion depends on neuronal activity in a parietooccipito-frontal network, which excludes the early stages of visual processing.