Bump attractor dynamics underlying stimulus integration in perceptual estimation tasks

Perceptual decision and continuous stimulus estimation tasks involve making judgments based on accumulated sensory evidence. Network models of evidence integration usually rely on competition between neural populations each encoding a discrete categorical choice. By design, these models do not maintain information of the integrated stimulus (e.g. the average stimulus direction in degrees) that is necessary for a continuous perceptual judgement. Here, we show that the continuous ring attractor network can integrate a stimulus feature such as orientation and track the stimulus average in the phase of its activity bump. We reduced the network dynamics of the ring model to a two-dimensional equation for the amplitude and the phase of the bump. Interestingly, these reduced equations are nearly identical to an optimal integration process for computing the running average of the stimulus orientation. They differ only in the intrinsic dynamics of the amplitude, which affects the temporal weighting of the sensory evidence. Whether the network shows early (primacy), uniform or late (recency) weighting depends on the relative strength of sensory stimuli compared to the amplitude of the bump and on the initial state of the network. The specific relation between the internal network dynamics and the sensory inputs can be modulated by changing a single parameter of the model, the global excitatory drive. We show that this can account for the heterogeneity of temporal weighting profiles observed in humans integrating a stream of oriented stimulus frames. Our findings point to continuous attractor dynamics as a plausible mechanism underlying stimulus integration in perceptual estimation tasks.

Effect of repetition on the behavioral and neuronal responses to ambiguous Necker cube images

A repeated presentation of an item facilitates its subsequent detection or identification, a phenomenon of priming. Priming may involve different types of memory and attention and affects neural activity in various brain regions. Here we instructed participants to report on the orientation of repeatedly presented Necker cubes with high (HA) and low (LA) ambiguity. Manipulating the contrast of internal edges, we varied the ambiguity and orientation of the cube. We tested how both the repeated orientation (referred to as a stimulus factor) and the repeated ambiguity (referred to as a top-down factor) modulated neuronal and behavioral response. On the behavioral level, we observed higher speed and correctness of the response to the HA stimulus following the HA stimulus and a faster response to the right-oriented LA stimulus following the right-oriented stimulus. On the neuronal level, the prestimulus theta-band power grew for the repeated HA stimulus, indicating activation of the neural networks related to attention and uncertainty processing. The repeated HA stimulus enhanced hippocampal activation after stimulus onset. The right-oriented LA stimulus following the right-oriented stimulus enhanced activity in the precuneus and the left frontal gyri before the behavioral response. During the repeated HA stimulus processing, enhanced hippocampal activation may evidence retrieving information to disambiguate the stimulus and define its orientation. Increased activation of the precuneus and the left prefrontal cortex before responding to the right-oriented LA stimulus following the right-oriented stimulus may indicate a match between their orientations. Finally, we observed increased hippocampal activation after responding to the stimuli, reflecting the encoding stimulus features in memory. In line with the large body of works relating the hippocampal activity with episodic memory, we suppose that this type of memory may subserve the priming effect during the repeated presentation of ambiguous images.

The responses of V1 cortical neurons to flashed presentations of orthogonal single lines and edges

How cortical neurons process multiple inputs is a fundamental issue in modern neuroscience. Neurons in visual cortical area V1 have been shown to exhibit cross-orientation suppression, where the response to an optimally oriented visual stimulus is reduced by the simultaneous presence of an orthogonally oriented stimulus. This is consistent with the view that cortical neurons respond to multiple inputs with a weighted average (or normalization) of the responses to the inputs presented separately. However, most of these studies have used drifting or counterphase-modulated grating stimuli, potentially confounding orientation effects with non-orientation-specific gain control mechanisms. Additionally, primate vision depends to a great extent on transient stimulus presentations during fixations between saccades. Therefore this study examined the responses of primate V1 neurons to orthogonal flashed-onset single edges and lines, and to their combinations. Single edges or lines do not typically cause strong suppression of the responses to an orthogonal stimulus, even though a grating does. This appears to hold true regardless of the relative contrasts of the orthogonal single lines or edges. This is consistent with response suppression from an orthogonal grating being due to non-orientation-specific contrast gain control (Koeling M, Shapley R, Shelley M. J Comp Neurosci 25: 390–400, 2008; Priebe NJ, Ferster D. Nat Neurosci 9: 552–561, 2006; Walker GA, Ohzawa I, Freeman RD. J.Neurophysiol 79: 227–239, 1998). While normalization mechanisms are clearly important for the cerebral cortex, under many conditions the responses of V1 cortical neurons to an optimally oriented stimulus can be unaffected by the presence of orthogonal stimuli, which may be important to avoid confounding the interpretation of a neural response.

Origins of Cross-Orientation Suppression in the Visual Cortex

The response of a neuron in striate cortex to an optimally oriented stimulus is suppressed by a superimposed orthogonal stimulus. The neural mechanism underlying this cross-orientation suppression (COS) may arise from intracortical or subcortical processes or from both. Recent studies of the temporal frequency and adaptation properties of COS suggest that depression at thalamo-cortical synapses may be the principal mechanism. To examine the possible role of synaptic depression in relation to COS, we measured the recovery time course of COS. We find it too rapid to be explained by synaptic depression. We also studied potential subcortical processes by measuring single cell contrast response functions for a population of LGN neurons. In general, contrast saturation is a consistent property of LGN neurons. Combined with rectifying nonlinearities in the LGN and spike threshold nonlinearities in visual cortex, contrast saturation in the LGN can account for most of the COS that is observed in the visual cortex.

Tilt Aftereffect and Adaptation-Induced Changes in Orientation Tuning in Visual Cortex

The tilt aftereffect (TAE) is a visual illusion in which prolonged adaptation to an oriented stimulus causes shifts in subsequent perceived orientations. Historically, neural models of the TAE have explained it as the outcome of response suppression of neurons tuned to the adapting orientation. Recent physiological studies of neurons in primary visual cortex (V1) have confirmed that such response suppression exists. However, it was also found that the preferred orientations of neurons shift away from the adapting orientation. Here we show that adding this second factor to a population coding model of V1 improves the correspondence between neurophysiological data and TAE measurements. According to our model, the shifts in preferred orientation have the opposite effect as response suppression, reducing the magnitude of the TAE.

Illuminant and Viewpoint Biases from Embossed Surfaces

The human visual system uses a-priori constraints for the estimation of surface shape from images. We propose here a robust paradigm to study individual observers' assumptions about the illuminant and viewpoint positions. In the study of illumination, the stimuli consisted of parallel, sinusoidally shaped, striped regions, alternating between wide and narrow. Narrow stripes alternating between white and black separated the uniform grey stripes, representing slanted edges in light and in shadow. The stimulus had the shape-from-shading ambiguity: either the wide or the narrow stripes could be seen as ‘in-front’, consistent with different assumed tilts of the illuminant. In a brief flash of a randomly oriented stimulus, observers stated whether the narrow or wide stripes appeared in the foreground. The results showed a strong bias for a light-from-above-left assumption (as in Howard et al, 1990 Perception19 523 – 530; Sun and Perona, 1996 Investigative Ophthalmology and Visual Science37 935). This bias was 20 to 30 deg to the left of vertical. Slower reaction times were obtained for more ambiguous figures. The same shape judgment task was used with an unshaded stimulus where the only depth cue was image contour. The same curvy, striped figure was portrayed with image contours at the edges of the stripes, as well as surface markings orthogonal to the depth variation, resulting in a shape-from-contour cue. We have previously reported indirect evidence for a bias of viewpoint above the object, that is observers interpret surface normals as pointing upward (Mamassian, 1995 Perception24 Supplement, 35). Our observers' shape judgments were consistent with this bias.