An Anatomical Substrate for the Spatiotemporal Transformation

Katnani HA, Gandhi NJ. Order of operations for decoding superior colliculus activity for saccade generation. J Neurophysiol 106: 1250-1259, 2011. First published June 15, 2011 doi:10.1152/jn.00265.2011To help understand the order of events that occurs when generating saccades, we simulated and tested two commonly stated decoding models that are believed to occur in the oculomotor system: vector averaging (VA) and center-of-mass. To generate accurate saccades, each model incorporates two required criteria: 1) a decoding mechanism that deciphers a population response of the superior colliculus (SC) and 2) an exponential transformation that converts the saccade vector into visual coordinates. The order of these two criteria is used differently within each model, yet the significance of the sequence has not been quantified. To distinguish between each decoding sequence and hence, to determine the order of events necessary to generate accurate saccades, we simulated the two models. Distinguishable predictions were obtained when two simultaneous motor commands are processed by each model. Experimental tests of the models were performed by observing the distribution of endpoints of saccades evoked by weighted, simultaneous microstimulation of two SC sites. The data were consistent with the predictions of the VA model, in which exponential transformation precedes the decoding computation.sequence of decoding; dual microstimulation; vector averaging; vector summation; center-of-mass THE SUPERIOR COLLICULUS (SC) is a critical, subcortical hub that plays a major role in converting sensory information into a motor command for saccade generation (Gandhi and Katnani 2011;Sparks 1986). Visual information in the SC is organized topographically in a logarithmic manner. A disproportionately large amount of SC tissue is allocated for (para-) foveal space and small-amplitude saccades, whereas a compressed region is attributed for the visual periphery and large-amplitude saccades (Cynader and Berman 1972;Robinson 1972). With the presentation of a stimulus, a population of neurons becomes active at a locus that represents the vector between the stimuli and line of sight (Wurtz and Goldberg 1972). Under ordinary circumstances, a comparable population discharges a highfrequency premotor burst to produce a saccade of the appropriate displacement (Sparks et al. 1976). To make certain that the saccadic eye movement lands near the desired location, two critical operations must be performed. One, the population response must be decoded using standard decoding mechanisms such as averaging or summation. Two, the SC output must undergo an exponential transformation to convert the saccade vector into visual coordinates (Ottes et al. 1986), the inverse transformation used to map visual space into SC coordinates. Studies have implemented the order of these two operations in different fashions. To the best of our knowledge, no attempt has been made to distinguish the order of these operations.In one scheme, the exponential transformation is applie...

Section: Interpretation Of Stimulation Resultsmentioning

confidence: 99%

“…Projections from the SC to the burst generator are weighted according to the site of origin (Moschovakis et al 1998). Specifically, the efficacy of the projections increases for neurons originating from regions encoding increasingly larger amplitude vectors.…”

Section: Neural Implementation Of Decoding Mechanismsmentioning

confidence: 99%

Order of operations for decoding superior colliculus activity for saccade generation

Katnani

Gandhi²

2011

“…Scudder et al (1996) used intracellular staining in alert squirrel monkeys to show that LLBNs in the rostral pons form at least two groups: one, located in the nrtp, is precerebellar like those of Crandall and Keller (1985); the other, located more dorsally in the rostral pons, projects to EBN areas. While the second group might subserve the serial processing hypothesized by Hepp and Henn (1983), recent anatomical evidence (Moschovakis et al 1998) does not support the notion of cell-to-cell processing. Instead, it suggests a differential organization of projections and terminal density (cf.…”

Section: Introductionmentioning

confidence: 89%

Saccade-Related, Long-Lead Burst Neurons in the Monkey Rostral Pons

Kaneko

2006

The paramedian pontine reticular formation contains the premotoneuronal cell groups that constitute the saccadic burst generator and control saccadic eye movements. Despite years of study and numerous investigations, the rostral portion of this area has received comparatively little attention, particularly the cell type known as long-lead burst neurons (LLBNs). Several hypotheses about the functional role of LLBNs in saccade generation have been proposed, although there is little information with which to assess them. To address this issue, I mapped and recorded LLBNs in the rostral pons to measure their discharge characteristics and correlate those characteristics with the metrics of the concurrent saccades. On the basis of their discharge and location, I identified three types of LLBNs in the rostral pons: excitatory (eLLBN), dorsal (dLLBN), and nucleus reticularis tegmenti pontis (nrtp) LLBNs. The eLLBNs, encountered throughout the pons, discharge for ipsilateral saccades in proportion to saccade amplitude, velocity, and duration. The dLLBNs, found at the pontomesencephalic junction, discharge maximally for ipsilateral saccades of a particular amplitude, usually <10°, and are not associated with a particular anatomical nucleus. The nrtp LLBNs, previously described as vector LLBNs, discharge for saccades of a particular direction and sometimes a particular amplitude. The discharge of the eLLBNs suggests they drive motor neurons. The anatomical projections of the nrtp LLBNs suggest that their involvement in saccade production is less direct. The discharge of dLLBNs is consistent with a role in providing the "trigger" signal that initiates saccades.

“…The resulting estimates of the SC firing patterns in space and time were subsequently decomposed into dynamic horizontal and vertical movement commands. In line with neuroanatomical data (Chimoto et al 1996;Moschovakis et al 1998;Scudder et al 1996), we used the efferent mapping function Van Gisbergen et al 1987) that assumes that SC neurons excite horizontal and vertical burst neurons in the brain stem with weights that are a function of their position in the SC motor map. The scheme in Fig.…”

Section: Reading the Population Codementioning

confidence: 99%

Dynamic Ensemble Coding of Saccades in the Monkey Superior Colliculus

Goossens

Opstal²

2006

225

. The deeper layers of the midbrain superior colliculus (SC) contain a topographic motor map in which a localized population of cells is recruited for each saccade, but how the brain stem decodes the dynamic SC output is unclear. Here we analyze saccade-related responses in the monkey SC to test a new dynamic ensemble-coding model, which proposes that each spike from each saccade-related SC neuron adds a fixed, site-specific contribution to the intended eye movement command. As predicted by this simple theory, we found that the cumulative number of spikes in the cell bursts is tightly related to the displacement of the eye along the ideal straight trajectory, both for normal saccades and for strongly curved, blink-perturbed saccades toward a single visual target. This dynamic relation depends systematically on the metrics of the saccade displacement vector, and can be fully predicted from a quantitative description of the cell's classical movement field. Furthermore, we show that a linear feedback model of the brain stem, which is driven by dynamic linear vector summation of measured SC firing patterns, produces realistic two-dimensional (2D) saccade trajectories and kinematics. We conclude that the SC may act as a nonlinear, vectorial saccade generator that programs an optimal straight eye-movement trajectory. I N T R O D U C T I O NThe midbrain superior colliculus (SC) is a sensorimotor interface that is critically involved in the control of rapid gaze shifts. An important problem in understanding its role in gaze control is how the spatial distribution of movement-related activity in its motor map is ultimately transformed into the temporal code carried by motor neurons (Sparks and HartwichYoung 1989). In this study, we analyzed saccade-related responses in the monkey SC to test a new theoretical framework for the involvement of the SC in the generation of saccades in two dimensions (2D). First, we present a novel analysis of SC spike trains that provides evidence for dynamic vector summation of movement contributions provided by each spike of each cell in the active population. We then analyze the spatialtemporal distribution of SC activity. The results are used to test the predictions and emerging properties of our new ensemblecoding theory, which assumes dynamic, linear decoding of the SC population activity by the brain stem saccade generator. Finally, we propose and test a new quantitative description of dynamic SC movement fields that is implied by our theory. In what follows, we first explain why a new approach is called for by highlighting the main findings that have led to several controversies. These controversies include 1) static versus dynamic involvement of the SC, 2) vector summation versus vector averaging of the population activity, and 3) feedforward versus feedback involvement of the SC. Earlier theories and controversies