Wilsaan M. Joiner

Long-Term Retention Explained by a Model of Short-Term Learning in the Adaptive Control of Reaching

Extensive theoretical, psychophysical, and neurobiological work has focused on the mechanisms by which short-term learning develops into long-term memory. Better understanding of these mechanisms may lead to the ability to improve the efficiency of training procedures. A key phenomenon in the formation of long-term memory is the effect of over learning on retention-discovered by Ebbinghaus in 1885: when the initial training period in a task is prolonged even beyond what is necessary for good immediate recall, long-term retention improves. Although this over learning effect has received considerable attention as a phenomenon in psychology research, the mechanisms governing this process are not well understood, and the ability to predict the benefit conveyed by varying degrees of over learning does not yet exist. Here we studied the relationship between the duration of an initial training period and the amount of retention 24 h later for the adaptation of human reaching arm movements to a novel force environment. We show that in this motor adaptation task, the amount of long-term retention is predicted not by the overall performance level achieved during the training period but rather by the level of a specific component process in a multi-rate model of short-term memory formation. These findings indicate that while multiple learning processes determine the ability to learn a motor adaptation, only one provides a gateway to long-term memory formation. Understanding the dynamics of this key learning process may allow for the rational design of training and rehabilitation paradigms that maximize the long-term benefit of each session.

Neuronal mechanisms for visual stability: progress and problems

How our vision remains stable in spite of the interruptions produced by saccadic eye movements has been a repeatedly revisited perceptual puzzle. The major hypothesis is that a corollary discharge (CD) or efference copy signal provides information that the eye has moved, and this information is used to compensate for the motion. There has been progress in the search for neuronal correlates of such a CD in the monkey brain, the best animal model of the human visual system. In this article, we briefly summarize the evidence for a CD pathway to frontal cortex, and then consider four questions on the relation of neuronal mechanisms in the monkey brain to stable visual perception. First, how can we determine whether the neuronal activity is related to stable visual perception? Second, is the activity a possible neuronal correlate of the proposed transsaccadic memory hypothesis of visual stability? Third, are the neuronal mechanisms modified by visual attention and does our perceived visual stability actually result from neuronal mechanisms related primarily to the central visual field? Fourth, does the pathway from superior colliculus through the pulvinar nucleus to visual cortex contribute to visual stability through suppression of the visual blur produced by saccades?

The training schedule affects the stability, not the magnitude, of the interlimb transfer of learned dynamics

The way that a motor adaptation is trained, for example, the manner in which it is introduced or the duration of the training period, can influence its internal representation. However, recent studies examining the gradual versus abrupt introduction of a novel environment have produced conflicting results. Here we examined how these effects determine the effector specificity of motor adaptation during visually guided reaching. After adaptation to velocity-dependent dynamics in the right arm, we estimated the amount of adaptation transferred to the left arm, using error-clamp measurement trials to directly measure changes in learned dynamics. We found that a small but significant amount of generalization to the untrained arm occurs under three different training schedules: a short-duration (15 trials) abrupt presentation, a long-duration (160 trials) abrupt presentation, and a long-duration gradual presentation of the novel dynamic environment. Remarkably, we found essentially no difference between the amount of interlimb generalization when comparing these schedules, with 9-12% transfer of the trained adaptation for all three. However, the duration of training had a pronounced effect on the stability of the interlimb transfer: The transfer elicited from short-duration training decayed rapidly, whereas the transfer from both long-duration training schedules was considerably more persistent (<50% vs. >90% retention over the first 20 trials). These results indicate that the amount of interlimb transfer is similar for gradual versus abrupt training and that interlimb transfer of learned dynamics can occur after even a brief training period but longer training is required for an enduring effect.

Saccadic Corollary Discharge Underlies Stable Visual Perception

Saccadic eye movements direct the high-resolution foveae of our retinas toward objects of interest. With each saccade, the image jumps on the retina, causing a discontinuity in visual input. Our visual perception, however, remains stable. Philosophers and scientists over centuries have proposed that visual stability depends upon an internal neuronal signal that is a copy of the neuronal signal driving the eye movement, now referred to as a corollary discharge (CD) or efference copy. In the old world monkey, such a CD circuit for saccades has been identified extending from superior colliculus through MD thalamus to frontal cortex, but there is little evidence that this circuit actually contributes to visual perception. We tested the influence of this CD circuit on visual perception by first training macaque monkeys to report their perceived eye direction, and then reversibly inactivating the CD as it passes through the thalamus. We found that the monkeys perception changed; during CD inactivation, there was a difference between where the monkey perceived its eyes to be directed and where they were actually directed. Perception and saccade were decoupled. We established that the perceived eye direction at the end of the saccade was not derived from proprioceptive input from eye muscles, and was not altered by contextual visual information. We conclude that the CD provides internal information contributing to the brains creation of perceived visual stability. More specifically, the CD might provide the internal saccade vector used to unite separate retinal images into a stable visual scene. SIGNIFICANCE STATEMENT Visual stability is one of the most remarkable aspects of human vision. The eyes move rapidly several times per second, displacing the retinal image each time. The brain compensates for this disruption, keeping our visual perception stable. A major hypothesis explaining this stability invokes a signal within the brain, a corollary discharge, that informs visual regions of the brain when and where the eyes are about to move. Such a corollary discharge circuit for eye movements has been identified in macaque monkey. We now show that selectively inactivating this brain circuit alters the monkeys visual perception. We conclude that this corollary discharge provides a critical signal that can be used to unite jumping retinal images into a consistent visual scene.

Amplitudes and directions of individual saccades can be adjusted by corollary discharge.

There is strong evidence that the brain can use an internally generated copy of motor commands, a corollary discharge, to guide rapid sequential saccades. Much of this evidence comes from the double-step paradigm: after two briefly flashed visual targets have disappeared, the subject makes two sequential saccades to the targets. Recent studies on the monkey revealed that amplitude variations of the first saccade led to compensation by the second saccade, mediated by a corollary discharge. Here, we investigated whether such saccade-by-saccade compensation occurs in humans, and we made three new observations. First, we replicated previous findings from the monkey: following first saccade amplitude variations, the direction of the second saccade compensated for the error. Second, the change in direction of the second saccade followed variations in vertical as well as horizontal first saccades although the compensation following horizontal saccades was significantly more accurate. Third, by examining oblique saccades, we are able to show that first saccade variations are compensated by adjustment in saccade amplitude in addition to direction. Together, our results demonstrate that it is likely that a corollary discharge in humans can be used to adjust both saccade direction and amplitude following variations in individual saccades.

Linear Hypergeneralization of Learned Dynamics Across Movement Speeds Reveals Anisotropic, Gain-Encoding Primitives for Motor Adaptation

The ability to generalize learned motor actions to new contexts is a key feature of the motor system. For example, the ability to ride a bicycle or swing a racket is often first developed at lower speeds and later applied to faster velocities. A number of previous studies have examined the generalization of motor adaptation across movement directions and found that the learned adaptation decays in a pattern consistent with the existence of motor primitives that display narrow Gaussian tuning. However, few studies have examined the generalization of motor adaptation across movement speeds. Following adaptation to linear velocity-dependent dynamics during point-to-point reaching arm movements at one speed, we tested the ability of subjects to transfer this adaptation to short-duration higher-speed movements aimed at the same target. We found near-perfect linear extrapolation of the trained adaptation with respect to both the magnitude and the time course of the velocity profiles associated with the high-speed movements: a 69% increase in movement speed corresponded to a 74% extrapolation of the trained adaptation. The close match between the increase in movement speed and the corresponding increase in adaptation beyond what was trained indicates linear hypergeneralization. Computational modeling shows that this pattern of linear hypergeneralization across movement speeds is not compatible with previous models of adaptation in which motor primitives display isotropic Gaussian tuning of motor output around their preferred velocities. Instead, we show that this generalization pattern indicates that the primitives involved in the adaptation to viscous dynamics display anisotropic tuning in velocity space and encode the gain between motor output and motion state rather than motor output itself.

Eye movement sequence generation in humans: Motor or goal updating?

Saccadic eye movements are often grouped in pre-programmed sequences. The mechanism underlying the generation of each saccade in a sequence is currently poorly understood. Broadly speaking, two alternative schemes are possible: first, after each saccade the retinotopic location of the next target could be estimated, and an appropriate saccade could be generated. We call this the goal updating hypothesis. Alternatively, multiple motor plans could be pre-computed, and they could then be updated after each movement. We call this the motor updating hypothesis. We used McLaughlins intra-saccadic step paradigm to artificially create a condition under which these two hypotheses make discriminable predictions. We found that in human subjects, when sequences of two saccades are planned, the motor updating hypothesis predicts the landing position of the second saccade in two-saccade sequences much better than the goal updating hypothesis. This finding suggests that the human saccadic system is capable of executing sequences of saccades to multiple targets by planning multiple motor commands, which are then updated by serial subtraction of ongoing motor output.

Modulation of Shifting Receptive Field Activity In Frontal Eye Field by Visual Salience

In the monkey frontal eye field (FEF), the sensitivity of some neurons to visual stimulation changes just before a saccade. Sensitivity shifts from the spatial location of its current receptive field (RF) to the location of that field after the saccade is completed (the future field, FF). These shifting RFs are thought to contribute to the stability of visual perception across saccades, and in this study we investigated whether the salience of the FF stimulus alters the magnitude of FF activity. We reduced the salience of the usually single flashed stimulus by adding other visual stimuli. We isolated 171 neurons in the FEF of 2 monkeys and did experiments on 50 that had FF activity. In 30% of these, that activity was higher before salience was reduced by adding stimuli. The mean magnitude reduction was 16%. We then determined whether the shifting RFs were more frequent in the central visual field, which would be expected if vision across saccades were only stabilized for the visual field near the fovea. We found no evidence of any skewing of the frequency of shifting receptive fields (or the effects of salience) toward the central visual field. We conclude that the salience of the FF stimulus makes a substantial contribution to the magnitude of FF activity in FEF. In so far as FF activity contributes to visual stability, the salience of the stimulus is probably more important than the region of the visual field in which it falls for determining which objects remain perceptually stable across saccades.

Suppressive Surrounds of Receptive Fields In Monkey Frontal Eye Field

A critical step in determining how a neuron contributes to visual processing is determining its visual receptive field (RF). While recording from neurons in frontal eye field (FEF) of awake monkeys (Macaca mulatta), we probed the visual field with small spots of light and found excitatory RFs that decreased in strength from RF center to periphery. However, presenting stimuli with different diameters centered on the RF revealed suppressive surrounds that overlapped the previously determined excitatory RF and reduced responses by 84%, on average. Consequently, in that overlap area, stimulation produced excitation or suppression, depending on the stimulus. Strong stimulation of the RF periphery with annular stimuli allowed us to quantify this effect. A modified difference of Gaussians model that independently varied center and surround activation accounted for the nonlinear activity in the overlap area. Our results suggest that (1) the suppressive surrounds found in FEF are fundamentally the same as those in V1 except for the size and strength of excitatory and suppressive mechanisms, (2) methodically assaying suppressive surrounds in FEF is essential for correctly interpreting responses to large and/or peripheral stimuli and therefore understanding the effects of stimulus context, and (3) regulating the relative strength of the surround clearly changes neuronal responses and may therefore play a significant part in the neuronal changes resulting from visual attention and stimulus salience.

Modulation of Presaccadic Activity in the Frontal Eye Field by the Superior Colliculus

A cascade of neuronal signals precedes each saccadic eye movement to targets in the visual scene. In the cerebral cortex, this neuronal processing culminates in the frontal eye field (FEF), where neurons have bursts of activity before the saccade. This presaccadic activity is typically considered to drive downstream activity in the intermediate layers of the superior colliculus (SC), which receives direct projections from FEF. Consequently, the FEF activity is thought to be determined solely by earlier cortical processing and unaffected by activity in the SC. Recent evidence of an ascending path from the SC to FEF raises the possibility, however, that presaccadic activity in the FEF may also depend on input from the SC. Here we tested this possibility by recording from single FEF neurons during the reversible inactivation of SC. Our results indicate that presaccadic activity in the FEF does not require SC input: we never observed a significant reduction in FEF presaccadic activity when the SC was inactivated. Unexpectedly, in a third of experiments, SC inactivation elicited a significant increase in FEF presaccadic activity. The passive visual response of FEF neurons, in contrast, was virtually unaffected by inactivation of the SC. These findings show that presaccadic activity in the FEF does not originate in the SC but nevertheless may be influenced by modulatory signals ascending from the SC.