Role of intrinsic synaptic circuitry in collicular sensorimotor integration

The superficial gray layer of the superior colliculus contains a map that represents the visual field, whereas the underlying intermediate gray layer contains a vector map of the saccades that shift the direction of gaze. These two maps are aligned so that a particular region of the visual field is represented directly above the neurons that orient the highest acuity area of the retina toward that region. Although it has been proposed that the transmission of information from the visuosensory to the motor map plays an important role in the generation of visually guided saccades, experiments have failed to demonstrate any functional linkage between the two layers. We examined synaptic transmission between these layers in vitro by stimulating the superficial layer while using whole-cell patch-clamp methods to measure the responses of intermediate layer neurons. Stimulation of superficial layer neurons evoked excitatory postsynaptic currents in premotor cells. This synaptic input was columnar in organization, indicating that the connections between the layers link corresponding regions of the visuosensory and motor maps. Excitatory postsynaptic currents were large enough to evoke action potentials and often occurred in clusters similar in duration to the bursts of action potentials that premotor cells use to command saccades. Our results indicate the presence of functional connections between the superficial and intermediate layers and show that such connections could play a significant role in the generation of visually guided saccades.

Feature integration in pattern perception

The human visual system is able to effortlessly integrate local features to form our rich perception of patterns, despite the fact that visual information is discretely sampled by the retina and cortex. By using a novel perturbation technique, we show that the mechanisms by which features are integrated into coherent percepts are scale-invariant and nonlinear (phase and contrast polarity independent). They appear to operate by assigning position labels or “place tags” to each feature. Specifically, in the first series of experiments, we show that the positional tolerance of these place tags in foveal, and peripheral vision is about half the separation of the features, suggesting that the neural mechanisms that bind features into forms are quite robust to topographical jitter. In the second series of experiment, we asked how many stimulus samples are required for pattern identification by human and ideal observers. In human foveal vision, only about half the features are needed for reliable pattern interpolation. In this regard, human vision is quite efficient (ratio of ideal to real ≈ 0.75). Peripheral vision, on the other hand is rather inefficient, requiring more features, suggesting that the stimulus may be relatively underrepresented at the stage of feature integration.

Role for cells in the presupplementary motor area in updating motor plans.

Two motor areas are known to exist in the medial frontal lobe of the cerebral cortex of primates, the supplementary motor area (SMA) and the presupplementary motor area (pre-SMA). We report here on an aspect of cellular activity that characterizes the pre-SMA. Monkeys were trained to perform three different movements sequentially in a temporal order. The correct order was planned on the basis of visual information before its execution. A group of pre-SMA cells (n = 64, 25%) were active during a process when monkeys were required to discard a current motor plan and develop a plan appropriate for the next orderly movements. Such activity was not common in the SMA and not found in the primary motor cortex. Our data suggest a role of pre-SMA cells in updating motor plans for subsequent temporally ordered movements.

Spatial integration and cortical dynamics.

Cells in adult primary visual cortex are capable of integrating information over much larger portions of the visual field than was originally thought. Moreover, their receptive field properties can be altered by the context within which local features are presented and by changes in visual experience. The substrate for both spatial integration and cortical plasticity is likely to be found in a plexus of long-range horizontal connections, formed by cortical pyramidal cells, which link cells within each cortical area over distances of 6-8 mm. The relationship between horizontal connections and cortical functional architecture suggests a role in visual segmentation and spatial integration. The distribution of lateral interactions within striate cortex was visualized with optical recording, and their functional consequences were explored by using comparable stimuli in human psychophysical experiments and in recordings from alert monkeys. They may represent the substrate for perceptual phenomena such as illusory contours, surface fill-in, and contour saliency. The dynamic nature of receptive field properties and cortical architecture has been seen over time scales ranging from seconds to months. One can induce a remapping of the topography of visual cortex by making focal binocular retinal lesions. Shorter-term plasticity of cortical receptive fields was observed following brief periods of visual stimulation. The mechanisms involved entailed, for the short-term changes, altering the effectiveness of existing cortical connections, and for the long-term changes, sprouting of axon collaterals and synaptogenesis. The mutability of cortical function implies a continual process of calibration and normalization of the perception of visual attributes that is dependent on sensory experience throughout adulthood and might further represent the mechanism of perceptual learning.

Motion perception: seeing and deciding.

The primate visual system offers unprecedented opportunities for investigating the neural basis of cognition. Even the simplest visual discrimination task requires processing of sensory signals, formation of a decision, and orchestration of a motor response. With our extensive knowledge of the primate visual and oculomotor systems as a base, it is now possible to investigate the neural basis of simple visual decisions that link sensation to action. Here we describe an initial study of neural responses in the lateral intraparietal area (LIP) of the cerebral cortex while alert monkeys discriminated the direction of motion in a visual display. A subset of LIP neurons carried high-level signals that may comprise a neural correlate of the decision process in our task. These signals are neither sensory nor motor in the strictest sense; rather they appear to reflect integration of sensory signals toward a decision appropriate for guiding movement. If this ultimately proves to be the case, several fascinating issues in cognitive neuroscience will be brought under rigorous physiological scrutiny.

Visual motion perception.

The primate visual motion system performs numerous functions essential for survival in a dynamic visual world. Prominent among these functions is the ability to recover and represent the trajectories of objects in a form that facilitates behavioral responses to those movements. The first step toward this goal, which consists of detecting the displacement of retinal image features, has been studied for many years in both psychophysical and neurobiological experiments. Evidence indicates that achievement of this step is computationally straightforward and occurs at the earliest cortical stage. The second step involves the selective integration of retinal motion signals according to the object of origin. Realization of this step is computationally demanding, as the solution is formally underconstrained. It must rely--by definition--upon utilization of retinal cues that are indicative of the spatial relationships within and between objects in the visual scene. Psychophysical experiments have documented this dependence and suggested mechanisms by which it may be achieved. Neurophysiological experiments have provided evidence for a neural substrate that may underlie this selective motion signal integration. Together they paint a coherent portrait of the means by which retinal image motion gives rise to our perceptual experience of moving objects.