Wyeth Bair

Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey

How reliably do action potentials in cortical neurons encode information about a visual stimulus? Most physiological studies do not weigh the occurrences of particular action potentials as significant but treat them only as reflections of average neuronal excitation. We report that single neurons recorded in a previous study by Newsome et al. (1989; see also Britten et al. 1992) from cortical area MT in the behaving monkey respond to dynamic and unpredictable motion stimuli with a markedly reproducible temporal modulation that is precise to a few milliseconds. This temporal modulation is stimulus dependent, being present for highly dynamic random motion but absent when the stimulus translates rigidly.

The influence of fixational eye movements on the response of neurons in area MT of the macaque.

We analyzed the relationship between eye movements and neuronal responses recorded from area MT in alert monkeys trained to maintain visual fixation during the presentation of moving patterns. The monkeys made small saccades which moved the eyes with velocities that spanned the sensitivity range of MT neurons. The saccades evoked changes in the neuronal response that depended upon (1) the level of stimulus-evoked activity amidst which the saccade occurred and (2) the direction of the saccade relative to the preferred direction of the neuron. Most notably, saccades were able to suppress stimulus-evoked activity when they caused retinal image flow that opposed the neurons preference and were able to elicit a response or enhance weak activity when they caused flow in the neurons preferred direction. On average, the disturbance lasted 40 ms beginning about 40 ms following saccade onset. Using these parameters, we simulated synthetic spike trains from an imaginary pair of similarly tuned neurons and determined that the interneuronal correlation due to saccades should be negligible at all but the lowest ongoing firing rates. This conclusion was supported from our data by the observation that response variance for single MT spike trains was not measurably reduced during periods of stable gaze compared to periods when eye movement exceeded a stability criterion (0.1 deg during 0.5 s). While the intrusions caused by saccades are too short-lived and infrequent to account for the variability of MT neuronal response (counter to the finding in V1 of Gur et al., 1997), the clear directional signal that they carry in area MT suggests that motion perception is not blocked during saccades by suppression at early stages in the visual pathway.

Spike timing in the mammalian visual system.

Evidence is accumulating for the existence of mechanisms that create and detect synchrony among action potentials on short time scales both within and between neurons. Progress is most rapid in the retina, the lateral geniculate nucleus, and cortical slices, where signal flow is better understood or more manipulable. The debate over the functional relevance of spike timing in cortex has gained substance from new computational models but remains unresolved.

Adaptive temporal integration of motion in direction-selective neurons in macaque visual cortex.

Direction-selective neurons in the primary visual cortex (V1) and the extrastriate motion area MT/V5 constitute a critical channel that links early cortical mechanisms of spatiotemporal integration to downstream signals that underlie motion perception. We studied how temporal integration in direction-selective cells depends on speed, spatial frequency (SF), and contrast using randomly moving sinusoidal gratings and spike-triggered average (STA) analysis. The window of temporal integration revealed by the STAs varied substantially with stimulus parameters, extending farther back in time for slow motion, high SF, and low contrast. At low speeds and high SF, STA peaks were larger, indicating that a single spike often conveyed more information about the stimulus under conditions in which the mean firing rate was very low. The observed trends were similar in V1 and MT and offer a physiological correlate for a large body of psychophysical data on temporal integration. We applied the same visual stimuli to a model of motion detection based on oriented linear filters (a motion energy model) that incorporated an integrate-and-fire mechanism and found that it did not account for the neuronal data. Our results show that cortical motion processing in V1 and in MT is highly nonlinear and stimulus dependent. They cast considerable doubt on the ability of simple oriented filter models to account for the output of direction-selective neurons in a general manner. Finally, they suggest that spike rate tuning functions may miss important aspects of the neural coding of motion for stimulus conditions that evoke low firing rates.

Dynamics of Suppression in Macaque Primary Visual Cortex

The response of a neuron in primary visual cortex (V1) to an optimal stimulus in its classical receptive field (CRF) can be reduced by the presence of an orthogonal mask, a phenomenon known as cross-orientation suppression. The presence of a parallel stimulus outside the CRF can have a similar effect, in this case known as surround suppression. We used a novel stimulus to probe the time course of cross-orientation suppression and found that it is very fast, starting even before the response to optimal excitatory stimuli. However, it occurs with some delay after the offset response, considered to be a measure of the earliest excitatory signals that reach the CRF. We also examined the time course of response to a stimulus presented outside the CRF and found that cross-orientation suppression begins substantially earlier than surround suppression measured in the same cells. Together, these findings suggest that cross-orientation suppression is attributable to either direct feedforward signal paths to V1 neurons or a circuit involving fast local interneurons within V1. Feedback from higher cortical areas is implicated in surround suppression, but our results make this an implausible mechanism for cross-orientation suppression. We conclude that suppression from inside and outside the CRF occur through different mechanisms.

Visual receptive field organization

Increasingly systematic approaches to quantifying receptive fields in primary visual cortex, combined with inspired ideas about functional circuitry, non-linearities, and visual stimuli, are bringing new interest to classical problems. This includes the distinction and hierarchy between simple and complex cells, the mechanisms underlying the receptive field surround, and debates about optimal stimuli for mapping receptive fields. An important new problem arises from recent observations of stimulus-dependent spatial and temporal summation in primary visual cortex. It appears that the receptive field can no longer be considered unique, and we might have to relinquish this cherished notion as the embodiment of neuronal function in primary visual cortex.

Computing motion using analog VLSI vision chips: an experimental comparison among different approaches

We have designed, built and tested a number of analog CMOS VLSI circuits for computing 1-D motion from the time-varying intensity values provided by an array of on-chip phototransistors. We present experimental data for two such circuits and discuss their relative performance. One circuit approximates the correlation model while a second chip uses resistive grids to compute zero-crossings to be tracked over time by a separate digital processor. Both circuits integrate image acquisition with image processing functions and compute velocity in real time. For comparison, we also describe the performance of a simple motion algorithm using off-the-shelf digital components. We conclude that analog circuits implementing various correlation-like motion algorithms are more robust than our previous analog circuits implementing gradient-like motion algorithms.

Computing motion using analog VLSI vision chips: an experimental comparison among four approaches

The authors have designed, built and tested a number of analog CMOS VLSI circuits for computing 1D motion from the time-varying intensity values provided by an array of on-chip phototransistors. The authors present experimental data for three such circuits and discuss their relative performance. One circuit approximates the correlation model, one the gradient model, while a third chip uses resistive grids to compute zerocrossings to be tracked over time by a separate digital processor. All circuits integrate image acquisition with image processing functions and compute velocity in real time. Finally, for comparison, the authors also describe the performance of a simple motion algorithm using off-the-shelf components.<<ETX>>

Equiluminance Cells in Visual Cortical Area V4

We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These “equiluminance” cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature—some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4.

Real-time motion detection using an analog VLSI zero-crossing chip

The authors have designed and tested a one-dimensional 64 pixel, analog CMOS VLSI chip which localizes intensity edges in real-time. This device exploits on-chip photoreceptors and the natural filtering properties of resistive networks to implement a scheme similar to and motivated by the Difference of Gaussians (DOG) operator proposed by Marr and Hildreth (1980). The chip computes the zero-crossings associated with the difference of two exponential weighting functions and reports only those zero-crossings at which the derivative is above an adjustable threshold. A real-time motion detection system based on the zero- crossing chip and a conventional microprocessor provides linear velocity output over two orders of magnitude of light intensity and target velocity.