Neel T. Dhruv

Profound Contrast Adaptation Early in the Visual Pathway

Prior exposure to a moving grating of high contrast led to a substantial and persistent reduction in the contrast sensitivity of neurons in the lateral geniculate nucleus (LGN) of macaque. This slow contrast adaptation was potent in all magnocellular (M) cells but essentially absent in parvocellular (P) cells and neurons that received input from S cones. Simultaneous recordings of M cells and the potentials of ganglion cells driving them showed that adaptation originated in ganglion cells. As expected from the spatiotemporal tuning of M cells, adaptation was broadly tuned for spatial frequency and lacked orientation selectivity. Adaptation could be induced by high temporal frequencies to which cortical neurons do not respond, but not by low temporal frequencies that can strongly adapt cortical neurons. Our observations confirm that contrast adaptation occurs at multiple levels in the visual system, and they provide a new way to reveal the function and perceptual significance of the M pathway.

Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque

The response of a neuron in striate cortex to an optimally configured visual stimulus is generally reduced when the stimulus is enlarged to encroach on a suppressive region that surrounds its classical receptive field (CRF). To characterize the mechanism that gives rise to this suppression, we measured its spatiotemporal tuning, its susceptibility to contrast adaptation, and its capacity for interocular transfer. Responses to an optimally configured grating confined to the CRF were strongly suppressed by annular surrounding gratings drifting at a wide range of temporal and spatial frequencies (including spatially uniform fields) that extended from well below to well above the range that drives most cortical neurons. Suppression from gratings capable of driving cortical CRFs was profoundly reduced by contrast adaptation and showed substantial interocular transfer. Suppression from stimuli that lay outside the spatiotemporal passband of most cortical CRFs was relatively stronger when the stimulus on the CRF was of low contrast, was generally insusceptible to contrast adaptation, and showed little interocular transfer. Our findings point to the existence of two mechanisms of surround suppression: one that is prominent when high-contrast stimuli drive the CRF, is orientation selective, has relatively sharp spatiotemporal tuning, is binocularly driven, and can be substantially desensitized by adaptation; the other is relatively more prominent when low-contrast stimuli drive the CRF, has very broad spatiotemporal tuning, is monocularly driven, and is insusceptible to adaptation. Its character suggests an origin in the input layers of primary visual cortex, or earlier.

The Detection of Visual Contrast in the Behaving Mouse

The mouse is becoming a key species for research on the neural circuits of the early visual system. To relate such circuits to perception, one must measure visually guided behavior and ask how it depends on fundamental stimulus attributes such as visual contrast. Using operant conditioning, we trained mice to detect visual contrast in a two-alternative forced-choice task. After 3–4 weeks of training, mice performed hundreds of trials in each session. Numerous sessions yielded high-quality psychometric curves from which we inferred measures of contrast sensitivity. In multiple sessions, however, choices were influenced not only by contrast, but also by estimates of reward value and by irrelevant factors such as recent failures and rewards. This behavior was captured by a generalized linear model involving not only the visual responses to the current stimulus but also a bias term and history terms depending on the outcome of the previous trial. We compared the behavioral performance of the mice to predictions of a simple decoder applied to neural responses measured in primary visual cortex of awake mice during passive viewing. The decoder performed better than the animal, suggesting that mice might not use optimally the information contained in the activity of visual cortex.

Habituation Reveals Fundamental Chromatic Mechanisms in Striate Cortex of Macaque

Prolonged viewing of a chromatically modulated stimulus usually leads to changes in its appearance, and that of similar stimuli. These aftereffects of habituation have been thought to reflect the activity of two populations of neurons in visual cortex that have particular importance in color vision, one sensitive to red–green modulation, the other to blue–yellow, but they have not been identified. We show here, in recordings from macaque primary visual cortex (V1), that prolonged exposure to chromatic modulation reveals two fundamental mechanisms with distinctive chromatic signatures that match those of the mechanisms identified by perceptual observations. In nearly all neurons, these mechanisms contribute to both excitation and to regulatory gain controls, and as a result their habituation can have paradoxical effects on response. The mechanisms must be located near the input layers of V1, before their distinct chromatic signatures diffuse. Our observations suggest that the fundamental mechanisms do not give rise to two distinct L–M and S chromatic pathways. Rather, the mechanisms are better understood as stages in the elaboration of chromatic tuning, expressed in varying proportions in all cells in V1 (and beyond), and made accessible to physiological and perceptual investigation only through habituation.

Cascaded Effects of Spatial Adaptation in the Early Visual System

Summary Virtually all stages of the visual system exhibit adaptation: neurons adjust their responses based on the recent stimulus history. While some of these adjustments occur at specific stages, others may be inherited from earlier stages. How do adaptation effects cascade along the visual system? We measured spatially selective adaptation at two successive stages in the mouse visual system: visual thalamus (LGN) and primary visual cortex (V1). This form of adaptation affected both stages but in drastically different ways: in LGN it only changed response gain, while in V1 it also shifted spatial tuning away from the adaptor. These effects, however, are reconciled by a simple model whereby V1 neurons summate LGN inputs with a fixed, unadaptable weighting profile. These results indicate that adaptation effects cascade through the visual system, that this cascading can shape selectivity, and that the rules of integration from one stage to the next are not themselves adaptable.

Multiple Adaptable Mechanisms Early in the Primate Visual Pathway

We describe experiments that isolate and characterize multiple adaptable mechanisms that influence responses of orientation-selective neurons in primary visual cortex (V1) of anesthetized macaque (Macaca fascicularis). The results suggest that three adaptable stages of machinery shape neural responses in V1: a broadly tuned early stage and a spatio-temporally tuned later stage, both of which provide excitatory input, and a normalization pool that is also broadly tuned. The early stage and the normalization pool are revealed by adapting gratings that themselves fail to evoke a response from the neuron: either low temporal frequency gratings at the null orientation or gratings of any orientation drifting at high temporal frequencies. When effective, adapting stimuli that altered the sensitivity of these two mechanisms caused reductions of contrast gain and often brought about a paradoxical increase in response gain due to a relatively greater desensitization of the normalization pool. The tuned mechanism is desensitized only by stimuli well matched to a neurons receptive field. We could thus infer desensitization of the tuned mechanism by comparing effects obtained with adapting gratings of preferred and null orientation modulated at low temporal frequencies.

A New Code for Contrast in the Primate Visual Pathway

We characterize a hitherto undocumented type of neuron present in the regions bordering the principal layers of the macaque lateral geniculate nucleus. Neurons of this type were distinguished by a high and unusually regular maintained discharge that was suppressed by spatiotemporal modulation of luminance or chromaticity within the receptive field. The response to any effective stimulus was a reduction in discharge, reminiscent of the “suppressed-by-contrast” cells of the cat retina. To a counterphase-modulated grating, the response was a phase-insensitive suppression modulated at twice the stimulus frequency, implying a receptive field comprised of multiple mechanisms that generate rectifying responses. This distinctive nonlinearity makes the neurons well suited to computing a measure of contrast energy; such a signal might be important in regulating sensitivity early in visual cortex.

Visual response properties of V1 neurons projecting to V2 in macaque.

Visual area V2 of the primate cortex receives the largest projection from area V1. V2 is thought to use its striate inputs as the basis for computations that are important for visual form processing, such as signaling angles, object borders, illusory contours, and relative binocular disparity. However, it remains unclear how selectivity for these stimulus properties emerges in V2, in part because the functional properties of the inputs are unknown. We used antidromic electrical stimulation to identify V1 neurons that project directly to V2 (10% of all V1 neurons recorded) and characterized their electrical and visual responses. V2-projecting neurons were concentrated in the superficial and middle layers of striate cortex, consistent with the known anatomy of this cortico-cortical circuit. Most were fast conducting and temporally precise in their electrical responses, and had broad spike waveforms consistent with pyramidal regular-spiking excitatory neurons. Overall, projection neurons were functionally diverse. Most, however, were tuned for orientation and binocular disparity and were strongly suppressed by large stimuli. Projection neurons included those selective and invariant to spatial phase, with roughly equal proportions. Projection neurons found in superficial layers had longer conduction times, broader spike waveforms, and were more responsive to chromatic stimuli; those found in middle layers were more strongly selective for motion direction and binocular disparity. Collectively, these response properties may be well suited for generating complex feature selectivity in and beyond V2.