Population coding: a historical sketch.
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Biomedical subjects
Publications and source records attributed to J T McIlwain.
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Students of vision have long speculated about the functions of the distinct lamination of the lateral geniculate nucleus and the massive return projection from visual cortex to this thalamic structure. This paper proposes that these features of the visual system reflect, in part at least, its solution to a geometric problem inherent in binocular vision. Points in the visual quadrants are imaged on geometrically non-corresponding retinal points. Two such retinal loci, optically conjugate with a given visual point at one fixation distance or angle, will correspond to no single visual point at other fixation distances or angles. This raises potential problems for visual cortical neurons sensitive to a narrow range of binocular disparities. If these neurons are to function optimally at a variety of fixation distances and angles, their disparity tuning must be variable. It is suggested here that such dynamic disparity tuning is effected by the corticogeniculate projection acting on the segregated ocular representations in the geniculate laminae.
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This paper reviews evidence that the superior colliculus (SC) of the midbrain represents visual direction and certain aspects of saccadic eye movements in the distribution of activity across a population of cells. Accurate and precise eye movements appear to be mediated, in part at least, by cells of the SC that have large sensory receptive fields and/or discharge in association with a range of saccades. This implies that visual points or saccade targets are represented by patches rather than points of activity in the SC. Perturbation of the pattern of collicular discharge by focal inactivation modifies saccade amplitude and direction in a way consistent with distributed coding. Several models have been advanced to explain how such a code might be implemented in the colliculus. Evidence related to these hypotheses is examined and continuing uncertainties are identified.
Cells projecting into the commissure of the cat's superior colliculus were identified during extracellular recording by antidromic activation. Electrical stimulation of the ipsilateral optic tract evoked action potentials in the majority of commissural neurons. Response latencies of 1.4 +/- .5 ms (mean +/- S.D.) in a few cells indicated that some commissural neurons receive direct input from the axons of retinal Y-cells. Most commissural cells responded 5.9 +/- 1.9 ms (mean +/- S.D.) following optic tract shock, implying that the responsible pathway was composed of more slowly conducting axons or did not proceed directly to the colliculus. Results of previous studies of retinal inputs to cells in the deep tectal layers suggest that the later responses were mediated by an indirect Y pathway through the visual cortex.
Saccades evoked electrically from the deep layers of the superior colliculus have been examined in the alert cat with its head fixed. Amplitudes of the vertical and horizontal components varied linearly with the starting position of the eye. The slopes of the linear-regression lines provided an estimate of the sensitivity of these components to initial eye position. In observations on 29 sites in nine cats, the vertical and horizontal components of saccades evoked from a given site were rarely influenced to the same degree by initial eye position. For most sites, the horizontal component was more sensitive than the vertical component. Sensitivities of vertical and horizontal components were lowest near the representations of the horizontal and vertical meridians, respectively, of the collicular retinotopic map, but otherwise exhibited no systematic retinotopic dependence. Estimates of component amplitudes for saccades evoked from the center of the oculomotor range also diverged significantly from those predicted from the retinotopic map. The results of this and previous studies indicate that electrical stimulation of the cat's superior colliculus cannot yield a unique oculomotor map or one that is in register everywhere with the sensory retinotopic map. Several features of these observations suggest that electrical stimulation of the colliculus produces faulty activation of a saccadic control system that computes target position with respect to the head and that small and large saccades are controlled differently.
Eye movements were recorded with the scleral search coil method while striate cortex (area 17) was stimulated in alert cats with their heads fixed. Regardless of where stimulation was applied in the retinotopic map, eye position at the onset of stimulation strongly affected the amplitudes of evoked saccades, but had much less influence on their directions. Application of long stimulus trains evoked repeated saccades at all sites tested. Highly convergent or goal-directed saccades were not observed. Cortically evoked saccades appeared to habituate with repeated stimulation and had higher thresholds and longer latencies that those reported for saccades evoked from the superior colliculus. The directions of cortically evoked saccades generally agreed with those predicted from the retinotopic coordinates of the stimulus sites, but saccade amplitudes were usually lower than expected. It is suggested that these findings are consistent with certain characteristics of eye-head coordination in the cat's normal visual orienting behavior. The results are difficult to reconcile with the hypothesis that goal-directed saccades are a normal response to targets outside the cat's oculomotor range.
The trajectories of saccadic eye movements evoked electrically from many brain structures are dependent to some degree on the initial position of the eye. Under certain conditions, likely to occur in stimulation experiments, local feedback models of the saccadic system can yield eye movements which behave in this way. The models in question assume that an early processing stage adds an internal representation of eye position to retinal error to yield a signal representing target position with respect to the head. The saccadic system is driven by the difference between this signal and one representing the current position of the eye. Albano & Wurtz (1982) pointed out that lesions perturbing the computation of eye position with respect to the head can result in initial position dependence of visually evoked saccades. It is shown here that position-dependent saccades will also result if electrical stimulation evokes a signal equivalent to retinal error but fails to effect a complete addition of eye position to this signal. Also, when multiple or staircase saccades are produced, as during long stimulus trains, they will have identical directions but decrease progressively in amplitude by a factor related to the fraction of added eye position.
Electrical stimulation was carried out in the intermediate and deep gray layers of the superior colliculus in alert cats. The heads of the animals were fixed, and their eye movements were recorded with the scleral search coil method. Stimulation in the anterior two-thirds of the colliculus with long-duration pulse trains produced multiple saccades, as in the primate (45, 51), but their directions and amplitudes were influenced significantly by the initial position of the eye. Stimulation in the posterior part of the colliculus evoked saccades that appeared to be "goal-directed," whereas stimulation at the extreme caudal edge of the colliculus yielded centering saccades. These observations confirm previous reports of Roucoux and Crommelinck (48) and Guitton et al. (24). Saccades evoked during bilateral simultaneous stimulation of the superior colliculi were also dependent on the initial position of the eye. At certain relative intensities of stimulation on the two sides, saccades failed to occur when the eye was within a particular part of the oculomotor range. When the eye was outside this region, the same stimuli triggered an eye movement that drove the eye toward the zone of saccade failure. These findings indicate that saccadic commands resulting from focal collicular stimulation in the cat can be modified by information about current eye position. It is not certain where in the brain this occurs or by what neural mechanisms, but a local feedback model of the saccadic control system (46) can account for the main observations. The functional significance of these findings depends in large measure on the degree to which focal collicular stimulation reproduces naturally occurring patterns of neural activity.
A series of visuotopic maps has been prepared from recordings of electrical potentials related to W-cell afferent activity in the cat's superior colliculus. These maps clearly exhibit an expected exaggeration of the representation of the upper visual field, due to tilt of the retina's visual streak in the 'position of paralysis'. This asymmetry disappears when the visual field's coordinate system is rotated by an angle equal to the tilt of the axis of the nasal streak. Previously published maps, based on recordings from postsynaptic collicular units, have failed to reflect this tilt of the nasal visual streak, perhaps in part because the centers of unit receptive-fields are biased estimators of the retinal origin of axons terminating near a collicular recording site.
In the superior colliculi of cats anesthetized with ketamine, 84% of identified output cells of the deep layers could be driven by shocks to the contralateral optic disk, optic chiasm, or ipsilateral optic tract; 75% of these deep-layer cells had response latencies reflecting a polysynaptic influence of retinal Y-cells. Following large, acute lesions of the ipsilateral occipital cortex (including visual areas 17, 18, 19, and the posteromedial lateral suprasylvian area (PMLS), only 18% of deep-layer output cells were driven by electrical stimulation of the optic pathway and only 4% exhibited an indirect Y-cell influence. Thus, one or more of these visual areas may be important for the relay of retinal information, and particularly of Y-cell information, to the deep layers of the superior colliculus. This hypothesis is supported by the observation that intracortical stimulation in areas 17, 18, 19, and PMLS activated many cells of the ipsilateral, deep tectal layers at latencies consistent with those exhibited by the indirect Y-cell pathway. The distributions of activation latencies were similar to those observed in the superficial layers, raising the possibility that at least some of the cortical influence on the deep layers may be mediated by direct connections. Cells of the deep layers were more likely to be excited by a cortical stimulus that activated cells immediately above them in the superficial layers than by a stimulus that did not. This indicates that the functional connections between visual cortex and the deep collicular layers exhibit a topographic orderliness similar to that previously described for corticotectal projections to the superficial layers. These results provide further evidence that the visual cortex exerts a significant influence on cells of the deep collicular strata and that the pathways involved are capable of mediating the indirect, retinal Y-cell input to these neurons.
1. Synaptically mediated spread of excitation has been studied during microstimulation in the intermediate gray layer of the superior colliculus of cats anesthetized with ketamine. Antidromic activation was used to identify those neurons sending axons to or through the contralateral pontine reticular formation. 2. Current thresholds were dependent on pulse duration, train length, and distance from the cell to the stimulus site. Stimulation with four cathodal pulses, 0.5 ms in duration, 30 microA in intensity, delivered at 400 Hz, excited cells of the intermediated gray up to 2-3 mm from the stimulus site. The results suggest that at least half the output cells in a region about 3 mm in diameter were driven by this stimulus. 3. The extent of spread in the unanesthetized midpontine-pretrigeminal cat was as great as, or greater than, that in animals anesthetized with ketamine. 4. Quick eye movements were evoked in ketamine-anesthetized cats by 100-ms trains of 0.5-ms pulses delivered at 400 Hz. Current thresholds for eye movements ranged from 15 to 90 microA, with most falling below 25 microA. 5. These results suggest that intracollicular microstimulation, with stimuli commonly used in studies of electrically evoked saccades, is accompanied by widespread synaptic activation of the intermediate gray layer. Since the metrics of electrically evoked saccades seem, nonetheless, to depend primarily on the location of the stimulating electrode, information about amplitude and direction must somehow be encoded in the distribution of neuronal discharge. 6. One possible form of such a distributed coding mechanism is discussed. This model assumes that the spatial densities of cells projecting to vertical and horizontal pulse generators of the saccadic system vary systematically beneath the retinotopic collicular map. Signals to the pulse generators change in magnitude as the collicular discharge zone occupies different positions in the connectional gradients and engages the specific output systems in varying proportion.
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The largest receptive fields mapped during microelectrode penetrations through the upper strata of the cat's superior colliculus vary substantially in size and shape in different collicular regions. Previous work has shown that when these large fields are plotted in the retinotopic map of the colliculus, their profiles become elliptical and vary little in size and orientation over the central regions of the map. Such profiles are called the receptive field images (RFIs) in the visual coordinate system of the colliculus. Of particular interest here is the relationship of these RFIs to the region of the colliculus occupied by cell whose receptive fields include a common visual point. We call this region the point image in the colliculus. A straightforward geometric argument indicates that the point image in the upper collicular strata should have the same size, shape, and orientation as the RFIs of the large-field cells recorded here, if, indeed, these RFIs are translationally invariant as suggested by the earlier studies. The experiments reported here directly assessed the translational invariance of large-field RFIs in the superior colliculi of individual cats. The results support the previous inference that the profiles are oval with their long axes oriented mediolaterally. The mediolateral and anteroposterior dimensions of the profiles were about 2.7 and 2.0 mm, respectively, wherever they were measured in the central regions of the colliculus. Since the boundaries of the point images in the superficial strata must have similar shape and dimensions, these data indicate that a visual point is "seen" by collicular cells spread through a substantial fraction of the tissue receiving the projection of the contralateral visual field.
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Cells projecting rostrally from the cat's superior colliculus were identified by antidromic activation from the posterior thalamus. These cells occurred principally in the stratum griseum superficiale and stratum opticum, although some were also encountered in deeper laminae. The rostrally projecting neurons of the superficial laminae formed a heterogeneous group with respect to axonal conduction velocity, receptive field dimensions and special response properties, such as directional and velocity sensitivity. No correlation was detected between receptive field size and estimated axonal conduction velocity in these units. Cells with the smallest receptive fields, were rarely excited antidromically from the thalamus.
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