Michael J. Hawken

Contrast's effect on spatial summation by macaque V1 neurons

Stimulation outside the receptive field of a primary visual cortical (V1) neuron reveals intracortical neural interactions. However, previous investigators implicitly or explicitly considered the extent of cortical spatial summation and, therefore, the size of the classical receptive field to be fixed and independent of stimulus characteristics or of surrounding context. On the contrary, we found that the extent of spatial summation in macaque V1 neurons depended on contrast, and was on average 2.3-fold greater at low contrast. This adaptive increase in spatial summation at low contrast was seen in cells throughout V1 and was independent of surround inhibition.

Orientation selectivity in macaque V1: diversity and laminar dependence.

We studied the steady-state orientation selectivity of single neurons in macaque primary visual cortex (V1). To analyze the data, two measures of orientation tuning selectivity, circular variance and orientation bandwidth, were computed from the tuning curves. Circular variance is a global measure of the shape of the tuning curve, whereas orientation bandwidth is a local measure of the sharpness of the tuning curve around its peak. Circular variance in V1 was distributed broadly, indicating a great diversity of orientation selectivity. This diversity was also reflected in the individual cortical layers. However, there was a tendency for neurons with high circular variance, meaning low selectivity for orientation, to be concentrated in layers 4C, 3B, and 5. The relative variation of orientation bandwidth across the cortical layers was less than for circular variance, but it showed a similar laminar dependence. Neurons with large orientation bandwidth were found predominantly in layers 4C and 3B. There was a weak correlation between orientation selectivity and the level of spontaneous activity of the neurons. We also assigned a response modulation ratio for each cell, which is a measure of the linearity of spatial summation. Cells with low modulation ratios tended to have higher circular variance and bandwidth than those with high modulation ratios. These findings suggest a revision to the classical view that nonoriented receptive fields are principally found in layer 4C and the cytochrome oxidase-rich blobs in layer 2/3. Instead, a broad distribution of tuning selectivity is found in all cortical layers, and neurons that are weakly tuned for orientation are ubiquitous in V1 cortex.

The spatial transformation of color in the primary visual cortex of the macaque monkey

Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.

Temporal-frequency selectivity in monkey visual cortex

We investigated the dynamics of neurons in the striate cortex (V1) and the lateral geniculate nucleus (LGN) to study the transformation in temporal-frequency tuning between the LGN and V1. Furthermore, we compared the temporal-frequency tuning of simple with that of complex cells and direction-selective cells with nondirection-selective cells, in order to determine whether there are significant differences in temporal-frequency tuning among distinct functional classes of cells within V1. In addition, we compared the cells in the primary input layers of V1 (4a, 4c alpha, and 4c beta) with cells in the layers that are predominantly second and higher order (2, 3, 4b, 5, and 6). We measured temporal-frequency responses to drifting sinusoidal gratings. For LGN neurons and simple cells, we used the amplitude and phase of the fundamental response. For complex cells, the elevation of impulse rate (F0) to a drifting grating was the response measure. There is significant low-pass filtering between the LGN and the input layers of V1 accompanied by a small, 3-ms increase in visual delay. There is further low-pass filtering between V1 input layers and the second- and higher-order neurons in V1. This results in an average decrease in high cutoff temporal-frequency between the LGN and V1 output layers of about 20 Hz and an increase in average visual latency of about 12-14 ms. One of the most salient results is the increased diversity of the dynamic properties seen in V1 when compared to the cells of the lateral geniculate, possibly reflecting specialization of function among cells in V1. Simple and complex cells had distributions of temporal-frequency tuning properties that were similar to each other. Direction-selective and nondirection-selective cells had similar preferred and high cutoff temporal frequencies, but direction-selective cells were almost exclusively band-pass while nondirection-selective cells distributed equally between band-pass and low-pass categories. Integration time, a measure of visual delay, was about 10 ms longer for V1 than LGN. In V1 there was a relatively broad distribution of integration times from 40-80 ms for simple cells and 60-100 ms for complex cells while in the LGN the distribution was narrower.

Gain Modulation by Nicotine in Macaque V1

Acetylcholine is a ubiquitous cortical neuromodulator implicated in cognition. In order to understand the potential for acetylcholine to play a role in visual attention, we studied nicotinic acetylcholine receptor (nAChR) localization and function in area V1 of the macaque. We found nAChRs presynaptically at thalamic synapses onto excitatory, but not inhibitory, neurons in the primary thalamorecipient layer 4c. Furthermore, consistent with the release enhancement suggested by this localization, we discovered that nicotine increases responsiveness and lowers contrast threshold in layer 4c neurons. We also found that nAChRs are expressed by GABAergic interneurons in V1 but rarely by pyramidal neurons, and that nicotine suppresses visual responses outside layer 4c. All sensory systems incorporate gain control mechanisms, or processes which dynamically alter input/output relationships. We demonstrate that at the site of thalamic input to visual cortex, the effect of this nAChR-mediated gain is an enhancement of the detection of visual stimuli.

Dynamics of Orientation Selectivity in the Primary Visual Cortex and the Importance of Cortical Inhibition

To test theories of orientation selectivity in primary visual cortex (V1), we have done experiments to measure the dynamics of orientation tuning of single neurons in the V1 cortex of macaque monkeys. Based on our dynamics results, we propose that a V1 cells orientation selectivity is generated mainly by both tuned enhancement and global suppression. Enhancement near the preferred orientation is probably caused by feed-forward input from LGN (plus amplification by cortical-cortical interaction). Global suppression could be supplied by cortical inhibition. Additionally, in about 1/3 of V1 neurons (usually the most sharply tuned) there is tuned suppression, centered near the cells preferred orientation but broader than tuned enhancement. These mechanisms also can explain important features of steady-state selectivity in the V1 neuron population. Furthermore, similar neuronal mechanisms may be used generally throughout the cerebral cortex.

Color in the Cortex: single- and double-opponent cells

This is a review of the research during the past 25years on cortical processing of color signals. At the beginning of the period the modular view of cortical processing predominated. However, at present an alternative view, that color and form are linked inextricably in visual cortical processing, is more persuasive than it seemed in 1985. Also, the role of the primary visual cortex, V1, in color processing now seems much larger than it did in 1985. The re-evaluation of the important role of V1 in color vision was caused in part by investigations of human V1 responses to color, measured with functional magnetic resonance imaging, fMRI, and in part by the results of numerous studies of single-unit neurophysiology in non-human primates. The neurophysiological results have highlighted the importance of double-opponent cells in V1. Another new concept is population coding of hue, saturation, and brightness in cortical neuronal population activity.

Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys.

SummaryContrast sensitivity and orientation selectivity were measured for neurons in lamina IV of macaque striate cortex. Contrast sensitivity was determined for a range of spatial frequencies, using a staircase method. The stimuli were at the optimal orientation, direction and speed of drift for each neuron. The assignment of each recording site to a subdivision of lamina IV was made by histological reconstruction of each electrode penetration from sections reacted for cytochrome oxidase and stained for Nissl substance. Neurons in the magnocellular recipient zone of IVc (IVcα) have high contrast sensitivities, while those in the parvocellular recipient zone (IVcβ) have low contrast sensitivities. Both of the upper subdivisions of lamina IV (IVa and IVb) contain a mixture of neurons with high and low contrast sensitivities. There were orientation selective neurons within all subdivisions of lamina IV, even in IVc, whereas non-oriented neurons were found only in those subdivisions that receive a direct parvocellular geniculate input (IVa and IVcβ).

Receptive field structure of neurons in monkey primary visual cortex revealed by stimulation with natural image sequences

Probing the visual system with the ensemble of signals that occur in the natural environment may reveal aspects of processing that are not evident in the neural responses to artificial stimulus sets, such as conventional bars and sinusoidal gratings. However, unsolved is the question of how to use complex natural stimulation, many aspects of which the experimenter cannot completely specify, to study neural processing. Here a method is presented to investigate the structure of a neurons receptive field based on its response to movie clips and other stimulus ensembles. As a particular case, the technique provides an estimate of the conventional first-order receptive field of a neuron, similar to what can be obtained with other reverse-correlation schemes. This is demonstrated experimentally and with computer simulations. Our analysis also revealed that the receptive fields of both simple and complex cells had regions where image boundaries, independent of their contrast sign, would enhance or suppress the cells response. In some cases, these signals were tuned for the orientation of the boundary. This demonstrates for the first time that it might be feasible to investigate the receptive field structure of visual neurons from their responses to natural image sequences.

Entrainment to video displays in primary visual cortex of macaque and humans

Cathode ray tubes (CRTs) display images refreshed at high frequency, and the temporal waveform of each pixel is a luminance impulse only a few milliseconds long. Although humans are perceptually oblivious to this flicker, we show in V1 in macaque monkeys and in humans that extracellularly recorded action potentials (spikes) and visual-evoked potentials (VEPs) align with the video impulses, particularly when high-contrast stimuli are viewed. Of 91 single units analyzed in macaque with a 60 Hz video refresh, 29 cells (32%) significantly locked their firing to a uniform luminance display, but their number increased to 75 (82%) when high-contrast stimuli were shown. Of 92 cells exposed to a 100 Hz refresh, 21 (23%) significantly phase locked to high-contrast stimuli. Phase locking occurred in both input and output layers of V1 for simple and complex cells, regardless of preferred temporal frequency. VEPs recorded in humans showed significant phase locking to the video refresh in all seven observers. Like the monkey neurons, human VEPs more typically phase locked to stimuli containing spatial contrast than to spatially uniform stimuli. Phase locking decreased when the refresh rate was increased. Thus in humans and macaques phase locking to the high strobe frequency of a CRT is enhanced by a salient spatial pattern, although the perceptual impact is uncertain. We note that a billion people worldwide manage to watch TV without obvious distortion of their visual perception despite extraordinary phase locking of their V1s to a 50 or 60 Hz signal.