Saccadic adaptation to moving targets

Saccades are so called ballistic movements which are executed without online visual feedback. After each saccade the saccadic motor plan is modified in response to post-saccadic feedback with the mechanism of saccadic adaptation. The post-saccadic feedback is provided by the retinal position of the target after the saccade. If the target moves after the saccade, gaze may follow the moving target. In that case, the eyes are controlled by the pursuit system, a system that controls smooth eye movements. Although these two systems have in the past been considered as mostly independent, recent lines of research point towards many interactions between them. We were interested in the question if saccade amplitude adaptation is induced when the target moves smoothly after the saccade. Prior studies of saccadic adaptation have considered intra-saccadic target steps as learning signals. In the present study, the intra-saccadic target step of the McLaughlin paradigm of saccadic adaptation was replaced by target movement, and a post-saccadic pursuit of the target. We found that saccadic adaptation occurred in this situation, a further indication of an interaction of the saccadic system and the pursuit system with the aim of optimized eye movements.     

Ganzfeld Stimulation or Sleep Enhance Long Term Motor Memory Consolidation Compared to Normal Viewing in Saccadic Adaptation Paradigm

Adaptation of saccade amplitude in response to intra-saccadic target displacement is a type of implicit motor learning which is required to compensate for physiological changes in saccade performance. Once established trials without intra-saccadic target displacement lead to de-adaptation or extinction, which has been attributed either to extra-retinal mechanisms of spatial constancy or to the influence of the stable visual surroundings. Therefore we investigated whether visual deprivation (“Ganzfeld”-stimulation or sleep) can partially maintain this motor learning compared to free viewing of the natural surroundings. Thirty-five healthy volunteers performed two adaptation blocks of 100 inward adaptation trials – interspersed by an extinction block – which were followed by a two-hour break with or without visual deprivation (VD). Using additional adaptation and extinction blocks short and long (4 weeks) term memory of this implicit motor learning were tested. In the short term, motor memory tested immediately after free viewing was superior to adaptation performance after VD. In the long run, however, effects were opposite: motor memory and relearning of adaptation was superior in the VD conditions. This could imply independent mechanisms that underlie the short-term ability of retrieving learned saccadic gain and its long term consolidation. We suggest that subjects mainly rely on visual cues (i.e., retinal error) in the free viewing condition which makes them prone to changes of the visual stimulus in the extinction block. This indicates the role of a stable visual array for resetting adapted saccade amplitudes. In contrast, visual deprivation (GS and sleep), might train subjects to rely on extra-retinal cues, e.g., efference copy or prediction to remap their internal representations of saccade targets, thus leading to better consolidation of saccadic adaptation.     

Sensory processing of motor inaccuracy depends on previously performed movement and on subsequent motor corrections: a study of the saccadic system

When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.     

Cerebellar complex spikes multiplex complementary behavioral information

Purkinje cell (PC) discharge, the only output of cerebellar cortex, involves 2 types of action potentials, high-frequency simple spikes (SSs) and low-frequency complex spikes (CSs). While there is consensus that SSs convey information needed to optimize movement kinematics, the function of CSs, determined by the PC’s climbing fiber input, remains controversial. While initially thought to be specialized in reporting information on motor error for the subsequent amendment of behavior, CSs seem to contribute to other aspects of motor behavior as well. When faced with the bewildering diversity of findings and views unraveled by highly specific tasks, one may wonder if there is just one true function with all the other attributions wrong? Or is the diversity of findings a reflection of distinct pools of PCs, each processing specific streams of information conveyed by climbing fibers? With these questions in mind, we recorded CSs from the monkey oculomotor vermis deploying a repetitive saccade task that entailed sizable motor errors as well as small amplitude saccades, correcting them. We demonstrate that, in addition to carrying error-related information, CSs carry information on the metrics of both primary and small corrective saccades in a time-specific manner, with changes in CS firing probability coupled with changes in CS duration. Furthermore, we also found CS activity that seemed to predict the upcoming events. Hence PCs receive a multiplexed climbing fiber input that merges complementary streams of information on the behavior, separable by the recipient PC because they are staggered in time.

Purkinje cell (PC) discharge, the only output of cerebellar cortex, involves both high-frequency simple spikes and low-frequency complex spikes; the function of the latter, determined by a PC’s climbing fibre input, remains controversial. This study shows that PCs receive a multiplexed climbing fibre input that merges complementary streams of information relevant for behaviour.     

A model of the cerebellum in adaptive control of saccadic gain

 We review data showing that the cerebellum is required for adaptation of saccadic gain to repeated presentations of dual-step visual targets and thus, presumably, for providing adaptive corrections for the brainstem saccade generator in response to any error created by the open-loop saccadic system. We model the adaptability of the system in terms of plasticity of synapses from parallel fibers to Purkinje cells in cerebellar cortex, stressing the integration of cerebellar cortex and nuclei in microzones as the units for correction of motor pattern generators. We propose a model of the inferior olive as an error detector, and use a ‘window of eligibility’ to insure that error signals that elicit a corrective movement are used to adjust the original movement, not the secondary movement. In a companion paper we simulate this large, realistic network of neural-like units to study the complex spatiotemporal behavior of neuronal subpopulations implicated in the control and adaptation of saccades. Received: 25 November 1994/Accepted in revised form: 6 February 1996     

A spiking neural network model of the midbrain superior colliculus that generates saccadic motor commands

Single-unit recordings suggest that the midbrain superior colliculus (SC) acts as an optimal controller for saccadic gaze shifts. The SC is proposed to be the site within the visuomotor system where the nonlinear spatial-to-temporal transformation is carried out: the population encodes the intended saccade vector by its location in the motor map (spatial), and its trajectory and velocity by the distribution of firing rates (temporal). The neurons’ burst profiles vary systematically with their anatomical positions and intended saccade vectors, to account for the nonlinear main-sequence kinematics of saccades. Yet, the underlying collicular mechanisms that could result in these firing patterns are inaccessible to current neurobiological techniques. Here, we propose a simple spiking neural network model that reproduces the spike trains of saccade-related cells in the intermediate and deep SC layers during saccades. The model assumes that SC neurons have distinct biophysical properties for spike generation that depend on their anatomical position in combination with a center–surround lateral connectivity. Both factors are needed to account for the observed firing patterns. Our model offers a basis for neuronal algorithms for spatiotemporal transformations and bio-inspired optimal controllers.     

Spatiotopic visual maps revealed by saccadic adaptation in humans

Saccadic adaptation [1] is a powerful experimental paradigm to probe the mechanisms of eye movement control and spatial vision, in which saccadic amplitudes change in response to false visual feedback. The adaptation occurs primarily in the motor system [2, 3], but there is also evidence for visual adaptation, depending on the size and the permanence of the postsaccadic error [4-7]. Here we confirm that adaptation has a strong visual component and show that the visual component of the adaptation is spatially selective in external, not retinal coordinates. Subjects performed?a memory-guided, double-saccade, outward-adaptation task designed to maximize visual adaptation and to dissociate the visual and motor corrections. When the memorized saccadic target was in the same position (in external space) as that used in the adaptation training, saccade targeting was strongly influenced by adaptation (even if not matched in retinal or cranial position), but when in the same retinal or cranial but different external spatial position, targeting was unaffected by adaptation, demonstrating unequivocal spatiotopic selectivity. These results point to the existence of a spatiotopic neural representation for eye movement control that adapts in response to saccade error signals.     

End-Point Variability Is Not Noise in Saccade Adaptation

When each of many saccades is made to overshoot its target, amplitude gradually decreases in a form of motor learning called saccade adaptation. Overshoot is induced experimentally by a secondary, backwards intrasaccadic target step (ISS) triggered by the primary saccade. Surprisingly, however, no study has compared the effectiveness of different sizes of ISS in driving adaptation by systematically varying ISS amplitude across different sessions. Additionally, very few studies have examined the feasibility of adaptation with relatively small ISSs. In order to best understand saccade adaptation at a fundamental level, we addressed these two points in an experiment using a range of small, fixed ISS values (from 0° to 1° after a 10° primary target step). We found that significant adaptation occurred across subjects with an ISS as small as 0.25°. Interestingly, though only adaptation in response to 0.25° ISSs appeared to be complete (the magnitude of change in saccade amplitude was comparable to size of the ISS), further analysis revealed that a comparable proportion of the ISS was compensated for across conditions. Finally, we found that ISS size alone was sufficient to explain the magnitude of adaptation we observed; additional factors did not significantly improve explanatory power. Overall, our findings suggest that current assumptions regarding the computation of saccadic error may need to be revisited.     

剌激中缝背核压抑大鼠小脑浦肯野细胞对苔状...

In anaesthetized and paralyzed rats, the effect of dorsal raphe (DR) conditioning stimulation on cerebellar Purkinje cell (PC) responses to mossy fiber and climbing fiber inputs were examined. The main results are as follows: (1) Stimulation of cerebral sensorimotor cortex elicits widespread activation of mossy and climbing fiber inputs to PCs in contralateral VI and VII lobules of the cerebellum and generates two kinds of evoked responses, i.e. the simple spike (SS) and the complex spike (CS) responses with respectively a latency 8-25 and 12-30 ms. (2) These PC responses could be markedly suppressed by stimulation of DR at intensities which by themselves were subthreshold for directly affecting PC's spontaneous SS and CS activities. (3) This DR-induced depressive effects on evoked PC's SS and CS excitations could be attenuated or blocked by systemic administration of 5-HT receptor blocker methysergide. These results demonstrate that serotonergic fiber input from DR can suppress the efficacy of mossy and climbing fiber synaptic action on PC, or decrease the responsiveness of PC itself to afferent synaptic action. The findings of this study also suggest that the raphe-cerebellar serotonergic fiber afferent system may be involved in some of the important neuronal processing in the cerebellum.     

Effect of harmaline on the complex spike shape and depression time in cerebellar Purkinje cell discharge in rat postnatal ontogenesis

Functional relationship between wave form of complex spike (CS) and depression time of simple spike (SS) in discharge of cerebellar Purkinje cells was studied after their activation with afferent climbing fiber at different terms of postnatal ontogenesis in norm and after treatment with harmaline. The experiments were carried out on three age groups of Wistar rats: rat pups (2 weeks), the adult (4–6 months), and the old animals (22–26 months). It was established that the SS duration in norm was approximately equal in rat pups, adult, and old animals, whereas it markedly decreased form the young to the old animals during the SS depression in the Purkinje cell discharge. Frequency of small action potential (lAP) and their number in the Purkinje cell discharge were approximately equal in young rat pups and adult animals, while in old animals these parameters were higher, on average, by 30%. After administration of harmaline, all CS parameters in rat pups and old animals increased in parallel with the depression time elongation. In adult rats, harmaline did not produce statistically significant changes of the mean values of CS parameters, but an increase of the simple spike depression time was observed. The obtained results allow concluding that the SS wave form and the simple spike depression time in norm are functionally coupled and change with age. The effect of harmaline on the CS wave forms as well as on interrelation of the CS duration and the CS depression time in the Purkinje cell discharge was more pronounced at the early and the late stages of Wistar rat postnatal ontogenesis.     

Vision as oculomotor reward: cognitive contributions to the dynamic control of saccadic eye movements

Humans and other primates are equipped with a foveated visual system. As a consequence, we reorient our fovea to objects and targets in the visual field that are conspicuous or that we consider relevant or worth looking at. These reorientations are achieved by means of saccadic eye movements. Where we saccade to depends on various low-level factors such as a targets’ luminance but also crucially on high-level factors like the expected reward or a targets’ relevance for perception and subsequent behavior. Here, we review recent findings how the control of saccadic eye movements is influenced by higher-level cognitive processes. We first describe the pathways by which cognitive contributions can influence the neural oculomotor circuit. Second, we summarize what saccade parameters reveal about cognitive mechanisms, particularly saccade latencies, saccade kinematics and changes in saccade gain. Finally, we review findings on what renders a saccade target valuable, as reflected in oculomotor behavior. We emphasize that foveal vision of the target after the saccade can constitute an internal reward for the visual system and that this is reflected in oculomotor dynamics that serve to quickly and accurately provide detailed foveal vision of relevant targets in the visual field.     

Millisecond-Scale Motor Encoding in a Cortical Vocal Area

Studies of motor control have almost universally examined firing rates to investigate how the brain shapes behavior. In principle, however, neurons could encode information through the precise temporal patterning of their spike trains as well as (or instead of) through their firing rates. Although the importance of spike timing has been demonstrated in sensory systems, it is largely unknown whether timing differences in motor areas could affect behavior. We tested the hypothesis that significant information about trial-by-trial variations in behavior is represented by spike timing in the songbird vocal motor system. We found that neurons in motor cortex convey information via spike timing far more often than via spike rate and that the amount of information conveyed at the millisecond timescale greatly exceeds the information available from spike counts. These results demonstrate that information can be represented by spike timing in motor circuits and suggest that timing variations evoke differences in behavior.     

Systematic Regional Variations in Purkinje Cell Spiking Patterns

In contrast to the uniform anatomy of the cerebellar cortex, molecular and physiological studies indicate that significant differences exist between cortical regions, suggesting that the spiking activity of Purkinje cells (PCs) in different regions could also show distinct characteristics. To investigate this possibility we obtained extracellular recordings from PCs in different zebrin bands in crus IIa and vermis lobules VIII and IX in anesthetized rats in order to compare PC firing characteristics between zebrin positive (Z+) and negative (Z−) bands. In addition, we analyzed recordings from PCs in the A2 and C1 zones of several lobules in the posterior lobe, which largely contain Z+ and Z− PCs, respectively. In both datasets significant differences in simple spike (SS) activity were observed between cortical regions. Specifically, Z− and C1 PCs had higher SS firing rates than Z+ and A2 PCs, respectively. The irregularity of SS firing (as assessed by measures of interspike interval distribution) was greater in Z+ bands in both absolute and relative terms. The results regarding systematic variations in complex spike (CS) activity were less consistent, suggesting that while real differences can exist, they may be sensitive to other factors than the cortical location of the PC. However, differences in the interactions between SSs and CSs, including the post-CS pause in SSs and post-pause modulation of SSs, were also consistently observed between bands. Similar, though less strong trends were observed in the zonal recordings. These systematic variations in spontaneous firing characteristics of PCs between zebrin bands in vivo, raises the possibility that fundamental differences in information encoding exist between cerebellar cortical regions.     

Linear ensemble-coding in midbrain superior colliculus specifies the saccade kinematics

Recently, we proposed an ensemble-coding scheme of the midbrain superior colliculus (SC) in which, during a saccade, each spike emitted by each recruited SC neuron contributes a fixed minivector to the gaze-control motor output. The size and direction of this 'spike vector' depend exclusively on a cell's location within the SC motor map (Goossens and Van Opstal, in J Neurophysiol 95: 2326-2341, 2006). According to this simple scheme, the planned saccade trajectory results from instantaneous linear summation of all spike vectors across the motor map. In our simulations with this model, the brainstem saccade generator was simplified by a linear feedback system, rendering the total model (which has only three free parameters) essentially linear. Interestingly, when this scheme was applied to actually recorded spike trains from 139 saccade-related SC neurons, measured during thousands of eye movements to single visual targets, straight saccades resulted with the correct velocity profiles and nonlinear kinematic relations ('main sequence properties' and 'component stretching'). Hence, we concluded that the kinematic nonlinearity of saccades resides in the spatial-temporal distribution of SC activity, rather than in the brainstem burst generator. The latter is generally assumed in models of the saccadic system. Here we analyze how this behaviour might emerge from this simple scheme. In addition, we will show new experimental evidence in support of the proposed mechanism.     

Statistical characteristics of climbing fiber spikes necessary for efficient cerebellar learning

 Mean firing rates (MFRs), with analogue values, have thus far been used as information carriers of neurons in most brain theories of learning. However, the neurons transmit the signal by spikes, which are discrete events. The climbing fibers (CFs), which are known to be essential for cerebellar motor learning, fire at the ultra-low firing rates (around 1 Hz), and it is not yet understood theoretically how high-frequency information can be conveyed and how learning of smooth and fast movements can be achieved. Here we address whether cerebellar learning can be achieved by CF spikes instead of conventional MFR in an eye movement task, such as the ocular following response (OFR), and an arm movement task. There are two major afferents into cerebellar Purkinje cells: parallel fiber (PF) and CF, and the synaptic weights between PFs and Purkinje cells have been shown to be modulated by the stimulation of both types of fiber. The modulation of the synaptic weights is regulated by the cerebellar synaptic plasticity. In this study we simulated cerebellar learning using CF signals as spikes instead of conventional MFR. To generate the spikes we used the following four spike generation models: (1) a Poisson model in which the spike interval probability follows a Poisson distribution, (2) a gamma model in which the spike interval probability follows the gamma distribution, (3) a max model in which a spike is generated when a synaptic input reaches maximum, and (4) a threshold model in which a spike is generated when the input crosses a certain small threshold. We found that, in an OFR task with a constant visual velocity, learning was successful with stochastic models, such as Poisson and gamma models, but not in the deterministic models, such as max and threshold models. In an OFR with a stepwise velocity change and an arm movement task, learning could be achieved only in the Poisson model. In addition, for efficient cerebellar learning, the distribution of CF spike-occurrence time after stimulus onset must capture at least the first, second and third moments of the temporal distribution of error signals. Received: 28 January 2000 / Accepted in revised form: 2 August 2000     

Responses of collicular fixation neurons to gaze shift perturbations in head-unrestrained monkey reveal gaze feedback control

A prominent hypothesis in motor control is that endpoint errors are minimized because motor commands are updated in real time via internal feedback loops. We investigated in monkey whether orienting saccadic gaze shifts made in the dark with coordinated eye-head movements are controlled by feedback. We recorded from superior colliculus fixation neurons (SCFNs) that fired tonically during fixation and were silent during gaze shifts. When we briefly (相似文献   

Auditory-evoked spike firing in the lateral amygdala and Pavlovian fear conditioning: mnemonic code or fear bias?

Amygdala neuroplasticity has emerged as a candidate substrate for Pavlovian fear memory. By this view, conditional stimulus (CS)-evoked activity represents a mnemonic code that initiates the expression of fear behaviors. However, a fear state may nonassociatively enhance sensory processing, biasing CS-evoked activity in amygdala neurons. Here we describe experiments that dissociate auditory CS-evoked spike firing in the lateral amygdala (LA) and both conditional fear behavior and LA excitability in rats. We found that the expression of conditional freezing and increased LA excitability was neither necessary nor sufficient for the expression of conditional increases in CS-evoked spike firing. Rather, conditioning-related changes in CS-evoked spike firing were solely determined by the associative history of the CS. Thus, our data support a model in which associative activity in the LA encodes fear memory and contributes to the expression of learned fear behaviors.     

Enhanced motor unit rate coding with improvements in a force-matching task

These data describe improved modulation of discharge rates (rate coding) of first dorsal interosseous motor units throughout the acquisition of a complex force-matching skill involving isometric index finger abduction. In each of 15 consecutive trials, subjects attempted to match their force to a trajectory consisting of the sum of two sine waves (0.15 and 0.5 Hz) and random oscillations (overall mean force level ˜20% MVC). Reductions in root-mean-square (RMS) error of each subject’s force relative to the trajectory indicated substantial improvements in force-matching ability (F=33.8, p<0.001). With the acquisition of this new skill, there was increased amplitude modulation of muscular force near both dominant frequencies of the force-matching trajectory (F=10.6, p=0.008). The standard deviation and coefficient of variation of motor unit inter-spike intervals both decreased with improved performance indicating a general reduction in the amplitude of firing rate modulations (SD: F=18.69, p=0.001; CV: F=43.6, p<0.001). After skill acquisition, there was decreased firing rate modulation outside of the two dominant frequencies and increased amplitude of firing rate modulation at the higher of the two dominant frequencies (0.5 Hz, F=8.23, p=0.015). These findings indicate that improved precision of rate coding was a contributor to the acquisition of the new force-matching task. That the change in rate coding was frequency dependent suggests that factors other than frequency coding may contribute to the improved force matching at 0.15 Hz.     

Dependence of different spike sequences on the mean neuronal firing rate in the neocortex in vivo and in vitro

Neuronal spikes were recorded extracellularly in rabbit visual cortex in vivo (88 cells) and in surviving slices of guinea pig sensorimotor cortex in vitro (50 cells). Spike sequences (SS) with monotonically increasing (SS+) and decreasing (SS-) interspike intervals were detected. Relative number of spikes of SS in the recording was closely associated with SS generation. The relative number of spikes was plotted against the average firing rate, this function had a biphasic character with the critical point around 7 Hz. The rate of change in interspike duration (the slope) was virtually independent of the firing rate, but was significantly different in vivo and in vitro conditions for both SS+ (325 and 180 ms/s, respectively) and SS- (270 and 160 ms/s, respectively). By and large, in vivo and in vitro the spike sequence parameters depended in the average firing rate in the same manner. The role of the spike sequences in rhythmic and information processes in neocortex is discussed.     

Rhythmic Firing of Pedunculopontine Tegmental Nucleus Neurons in Monkeys during Eye Movement Task

The pedunculopontine tegmental nucleus (PPTN) has been thought to be involved in the control of behavioral state. Projections to the entire thalamus and reciprocal connections with the basal ganglia nuclei suggest a potential role for the PPTN in the control of various rhythmic behaviors, including waking/sleeping and locomotion. Recently, rhythmic activity in the local field potentials was recorded from the PPTN of patients with Parkinson''s disease who were treated with levodopa, suggesting that rhythmic firing is a feature of the functioning PPTN and might change with the behaving conditions even within waking. However, it remains unclear whether and how single PPTN neurons exhibit rhythmic firing patterns during various behaving conditions, including executing conditioned eye movement behaviors, seeking reward, or during resting. We previously recorded from PPTN neurons in healthy monkeys during visually guided saccade tasks and reported task-related changes in firing rate, and in this paper, we reanalyzed these data and focused on their firing patterns. A population of PPTN neurons demonstrated a regular firing pattern in that the coefficient of variation of interspike intervals was lower than what would be expected of theoretical random and irregular spike trains. Furthermore, a group of PPTN neurons exhibited a clear periodic single spike firing that changed with the context of the behavioral task. Many of these neurons exhibited a periodic firing pattern during highly active conditions, either the fixation condition during the saccade task or the free-viewing condition during the intertrial interval. We speculate that these task context-related changes in rhythmic firing of PPTN neurons might regulate the monkey''s attentional and vigilance state to perform the task.