Lance M. Optican

Distributed model of control of saccades by superior colliculus and cerebellum

We investigate the role that superior colliculus (SC) and cerebellum (CBLM) might play in controlling saccadic eye movements. Even though strong experimental evidence argues for an important role for the CBLM, the most recent models of the saccadic system have relied mostly on the SC for the dynamic control of saccades. In this study, we propose that saccades are controlled by two parallel pathways, one including the SC and the other including the CBLM. In this model, both SC and CBLM provide part of the drive to the saccade. Furthermore, the CBLM receives direct feedback from the brain stem and keeps track of the residual motor error, so that it can issue appropriate commands to compensate for incorrect heading and to end the movement when the target has been foveated. We present here a distributed model that produces realistic saccades and accounts for a great deal of neurophysiological data.

Superior colliculus neurons provide the saccadic motor error signal

SummaryStudies of the intermediate layers of the superior colliculus have suggested that it provides a desired change in eye position signal (ΔE) for the generation of saccadic eye movements. Recent evidence, however, has shown that some neurons in these layers may be related to the velocity of saccades. We present single cell recordings from the intermediate layers of monkey superior colliculus that are consistent with the hypothesis that many superior colliculus neurons provide instead a motor error signal, em. Our hypothesis about the function of these cells places them inside the local feedback loop controlling the waveform of the saccade.

A hypothetical explanation of congenital nystagmus

Congenital nystagmus (CN) is a conjugate, rhythmic, eye movement disorder characterized by a wide variety of waveforms ranging from jerk to pendular types. No detailed mechanisms have been proposed to explain the generation of the CN wave-form This paper proposes a hypothetical mechanism for CN, and shows with computer simulations that a model based on this hypothesis can account for a variety of disparate waveforms. The basis of this model is a gaze-holding network, or neural integrator, that has both position and velocity feedback loops. The signals carried in these loops could arise from either afference or efference. In normal subjects, the position feedback would be positive and the velocity feedback would be negative. Both would help to increase the time constant of an imperfect neural integrator in the brain stem. We propose that in patients with CN the sign of the velocity pathway is reversed, making the neural integrator unstable. This instability could manifest as many different CN waveforms, depending on the direction and velocity of post-saccadic ocular drift and actions of nonlinearities within the position and velocity feedback loops. Thus a single underlying abnormality may be responsible for a variety of CN waveforms.

The maintenance of spatial accuracy by the periasaccadic remapping of visual receptive fields

Humans and monkeys can direct their eyes to the spatial location of briefly flashed targets even when a saccade intervenes between the stimulus flash and the saccade to acquire its location. It had been proposed that the oculomotor system performs this task by resorting to a supraretinal representation of space. In this paper we review neurophysiological and clinical data suggesting that the brain can use a different strategy that does not require an explicit supraretinal representation of targets. We propose and implement a simple neural model that can keep track continuously of the location of saccade targets in eye-centered coordinates. Finally, based on recent data, we argue that such a neural mechanism is in fact used to keep track not only of saccade targets but of the location of salient areas of the visual scene in general.

Unbiased measures of transmitted information and channel capacity from multivariate neuronal data

Two measures from information theory, transmitted information and channel capacity, can quantify the ability of neurons to convey stimulus-dependent information. These measures are calculated using probability functions estimated from stimulus-response data. However, these estimates are biased by response quantization, noise, and small sample sizes. Improved estimators are developed in this paper that depend on both an estimate of the sample-size bias and the noise in the data.

Oculopalatal tremor explained by a model of inferior olivary hypertrophy and cerebellar plasticity

The inferior olivary nuclei clearly play a role in creating oculopalatal tremor, but the exact mechanism is unknown. Oculopalatal tremor develops some time after a lesion in the brain that interrupts inhibition of the inferior olive by the deep cerebellar nuclei. Over time the inferior olive gradually becomes hypertrophic and its neurons enlarge developing abnormal soma-somatic gap junctions. However, results from several experimental studies have confounded the issue because they seem inconsistent with a role for the inferior olive in oculopalatal tremor, or because they ascribe the tremor to other brain areas. Here we look at 3D binocular eye movements in 15 oculopalatal tremor patients and compare their behaviour to the output of our recent mathematical model of oculopalatal tremor. This model has two mechanisms that interact to create oculopalatal tremor: an oscillator in the inferior olive and a modulator in the cerebellum. Here we show that this dual mechanism model can reproduce the basic features of oculopalatal tremor and plausibly refute the confounding experimental results. Oscillations in all patients and simulations were aperiodic, with a complicated frequency spectrum showing dominant components from 1 to 3 Hz. The model’s synchronized inferior olive output was too small to induce noticeable ocular oscillations, requiring amplification by the cerebellar cortex. Simulations show that reducing the influence of the cerebellar cortex on the oculomotor pathway reduces the amplitude of ocular tremor, makes it more periodic and pulse-like, but leaves its frequency unchanged. Reducing the coupling among cells in the inferior olive decreases the oscillation’s amplitude until they stop (at ∼20% of full coupling strength), but does not change their frequency. The dual-mechanism model accounts for many of the properties of oculopalatal tremor. Simulations suggest that drug therapies designed to reduce electrotonic coupling within the inferior olive or reduce the disinhibition of the cerebellar cortex on the deep cerebellar nuclei could treat oculopalatal tremor. We conclude that oculopalatal tremor oscillations originate in the hypertrophic inferior olive and are amplified by learning in the cerebellum.

Cortical feedback increases visual information transmitted by monkey parvocellular lateral geniculate nucleus neurons

We studied the effect of cooling the striate cortex on parvocellular lateral geniculate nucleus (PLGN) neurons in awake monkeys. Cooling the striate cortex produced both facilitation and inhibition of the responses of all neurons, depending on the stimulus presented. Cooling the striate cortex also altered the temporal distribution of spikes in the responses of PLGN neurons. Shannons information measure revealed that cooling the striate cortex reduced the average stimulus-related information transmitted by all PLGN neurons. The reduction in transmitted information was associated with both facilitation and inhibition of the response. Cooling the striate cortex reduced the amount of information transmitted about all of the stimulus parameters tested: pattern, luminance, spatial contrast, and sequential contrast. The effect of cooling was nearly the same for codes based on the number of spikes in the response as for codes based on their temporal distribution. The reduction in transmitted information occurred because the differences among the responses to different stimuli (signal separation) were reduced, not because the variability of the responses to individual stimuli (noise) was increased. We conclude that one function of corticogeniculate feedback is to improve the ability of PLGN neurons to discriminate among stimuli by enhancing the differences among their responses.

Superior colliculus cell types and models of saccade generation.

Recent experiments on the cat and monkey have revealed several different cell types within the superior colliculus, including fixation, burst, and build up cells. During primate saccades, activity remains fixed at one location in burst cells, but spreads across the colliculus in build up cells. New models based on the activity of these cell types suggest their functional roles in saccade generation.

Involuntary attentional shifts due to orientation differences

We tested the ability of orientation differences to cause involuntary shifts of visual attention and found that these attentional shifts can occur in response to an orientation “pop-out” display. Texturelike cue stimuli consisting of discrete oriented bars, with either uniform orientation or containing a noninformative orthogonally oriented bar, were presented for a variable duration. Subsequent to or partially coincident with the cue stimulus was the target display of a localization or two-interval forced-choice task, followed by a mask display. Naive subjects consistently showed greater accuracy in trials with the target at the location of the orthogonal orientation compared with trials with uniformly oriented bars, with only 100 msec between the cue and mask onsets. Discriminating these orientations required a stimulus onset asynchrony (SOA) of 50–70 msec. The attentional facilitation is transient, in most cases absent, with a cue-mask SOA of 250 msec. These results suggest that the preattentive character of some texture discrimination tasks with SOAs of only 100 msec is vitiated by the involuntary attentional shifts that are caused by orientation differences.

A field theory of saccade generation: temporal-to-spatial transform in the superior colliculus

Recent models have placed the superior colliculus inside the local feedback loop that generates the pulse of innervation needed to make a saccade. Such closed-loop models need to take into account the different coordinate systems of visual and motor signals. This paper presents a computational model showing how the superior colliculus can bring the visual and motor information together in a common reference frame.