Dataset Information

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus.

ABSTRACT: A major challenge in computational neurobiology is to understand how populations of noisy, broadly-tuned neurons produce accurate goal-directed actions such as saccades. Saccades are high-velocity eye movements that have stereotyped, nonlinear kinematics; their duration increases with amplitude, while peak eye-velocity saturates for large saccades. Recent theories suggest that these characteristics reflect a deliberate strategy that optimizes a speed-accuracy tradeoff in the presence of signal-dependent noise in the neural control signals. Here we argue that the midbrain superior colliculus (SC), a key sensorimotor interface that contains a topographically-organized map of saccade vectors, is in an ideal position to implement such an optimization principle. Most models attribute the nonlinear saccade kinematics to saturation in the brainstem pulse generator downstream from the SC. However, there is little data to support this assumption. We now present new neurophysiological evidence for an alternative scheme, which proposes that these properties reside in the spatial-temporal dynamics of SC activity. As predicted by this scheme, we found a remarkably systematic organization in the burst properties of saccade-related neurons along the rostral-to-caudal (i.e., amplitude-coding) dimension of the SC motor map: peak firing-rates systematically decrease for cells encoding larger saccades, while burst durations and skewness increase, suggesting that this spatial gradient underlies the increase in duration and skewness of the eye velocity profiles with amplitude. We also show that all neurons in the recruited population synchronize their burst profiles, indicating that the burst-timing of each cell is determined by the planned saccade vector in which it participates, rather than by its anatomical location. Together with the observation that saccade-related SC cells indeed show signal-dependent noise, this precisely tuned organization of SC burst activity strongly supports the notion of an optimal motor-control principle embedded in the SC motor map as it fully accounts for the straight trajectories and kinematic nonlinearity of saccades.

SUBMITTER: Goossens HH

PROVIDER: S-EPMC3355059 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus.

Goossens H H L M HH van Opstal A J AJ

PLoS computational biology 20120517 5

A major challenge in computational neurobiology is to understand how populations of noisy, broadly-tuned neurons produce accurate goal-directed actions such as saccades. Saccades are high-velocity eye movements that have stereotyped, nonlinear kinematics; their duration increases with amplitude, while peak eye-velocity saturates for large saccades. Recent theories suggest that these characteristics reflect a deliberate strategy that optimizes a speed-accuracy tradeoff in the presence of signal-d ...[more]

PMID: 22615548

Similar Datasets

Project description:Following the suggestion that a command encoding current target location feeds the oculomotor system during interceptive saccades, we tested the involvement of the deep superior colliculus (dSC). Extracellular activity of 52 saccade-related neurons was recorded in three monkeys while they generated saccades to targets that were static or moving along the preferred axis, away from (outward) or toward (inward) a fixated target with a constant speed (20°/s). Vertical and horizontal motions were tested when possible. Movement field (MF) parameters (boundaries, preferred vector, and firing rate) were estimated after spline fitting of the relation between the average firing rate during the motor burst and saccade amplitude. During radial target motions, the inner MF boundary shifted in the motion direction for some, but not all, neurons. Likewise, for some neurons, the lower boundaries were shifted upward during upward motions and the upper boundaries downward during downward motions. No consistent change was observed during horizontal motions. For some neurons, the preferred vectors were also shifted in the motion direction for outward, upward, and "toward the midline" target motions. The shifts of boundary and preferred vector were not correlated. The burst firing rate was consistently reduced during interceptive saccades. Our study demonstrates an involvement of dSC neurons in steering the interceptive saccade. When observed, the shifts of boundary in the direction of target motion correspond to commands related to past target locations. The absence of shift in the opposite direction implies that dSC activity does not issue predictive commands related to future target location.NEW & NOTEWORTHY The deep superior colliculus is involved in steering the saccade toward the current location of a moving target. During interceptive saccades, the active population consists of a continuum of cells ranging from neurons issuing commands related to past locations of the target to neurons issuing commands related to its current location. The motor burst of collicular neurons does not contain commands related to the future location of a moving target.

Project description:The superior colliculus (SC) and pulvinar are thought to function as a subcortical visual pathway that bypasses the striate cortex and detects fundamental facial information. We previously investigated neuronal responses in the SC and pulvinar of monkeys during a delayed nonmatching-to-sample task, in which the monkeys were required to discriminate among 35 facial photos of five models and other categories of visual stimuli, and reported that population coding by multiple SC and pulvinar neurons well discriminated facial photos from other categories of stimuli (Nguyen et al., 2013, 2014). However, it remains unknown whether population coding could represent multiple types of facial information including facial identity, gender, facial orientation, and gaze direction. In the present study, to investigate population coding of multiple types of facial information by the SC and pulvinar neurons, we reanalyzed the same neuronal responses in the SC and pulvinar; the responses of 112 neurons in the SC and 68 neurons in the pulvinar in serial 50-ms epochs after stimulus onset were reanalyzed with multidimensional scaling (MDS). The results indicated that population coding by neurons in both the SC and pulvinar classified some aspects of facial information, such as face orientation, gender, and identity, of the facial photos in the second epoch (50-100 ms after stimulus onset). The Euclidean distances between all the pairs of stimuli in the MDS spaces in the SC were significantly correlated with those in the pulvinar, which suggested that the SC and pulvinar function as a unit. However, in contrast with the known population coding of face neurons in the temporal cortex, the facial information coding in the SC and pulvinar was coarse and insufficient. In these subcortical areas, identity discrimination was face orientation-dependent and the left and right profiles were not discriminated. Furthermore, gaze direction information was not extracted in the SC and pulvinar. These results suggest that the SC and pulvinar, which comprise the subcortical visual pathway, send coarse and rapid information on faces to the cortical system in a bottom-up process.

Dataset Information

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus.

Publications

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets