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.
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.
Summary The local field potential (LFP) is increasingly used to measure the combined activity of neurons within a region of tissue. Yet, available estimates of the size of this region are highly disparate, ranging from a few hundred microns to several millimeters. To measure the size of this region directly, we used a combination of multielectrode recordings and optical imaging. We determined the orientation selectivity of stimulus-evoked LFP signals in cat area V1 and were able to predict it on the basis of the surrounding map of orientation preference. The results show that LFP signals originate within ~250 μm of the recording electrode. This quantitative estimate of spatial scale indicates that LFPs are more local than often recognized, and provides a guide to the interpretation of the increasing number of studies that rest on LFP recordings.
I present measurements of the spatial structure of simple-cell receptive fields in macaque primary visual cortex (area V1). Similar to previous findings in cat area 17, the spatial profile of simple-cell receptive fields in the macaque is well described by two-dimensional Gabor functions. A population analysis reveals that the distribution of spatial profiles in primary visual cortex lies approximately on a one-parameter family of filter shapes. Surprisingly, the receptive fields cluster into even- and odd-symmetry classes with a tendency for neurons that are well tuned in orientation and spatial frequency to have odd-symmetric receptive fields. The filter shapes predicted by two recent theories of simple-cell receptive field function, independent component analysis and sparse coding, are compared with the data. Both theories predict receptive fields with a larger number of subfields than observed in the experimental data. In addition, these theories do not generate receptive fields that are broadly tuned in orientation and low-pass in spatial frequency, which are commonly seen in monkey V1. The implications of these results for our understanding of image coding and representation in primary visual cortex are discussed.
Neurons in visual cortex are linked by an extensive network of lateral connections. To study the effect of these connections on neural responses, we recorded spikes and local field potentials (LFPs) from multi-electrode arrays that were implanted in monkey and cat primary visual cortex. Spikes at each location generated outward traveling LFP waves. When the visual stimulus was absent or had low contrast, these LFP waves had large amplitudes and traveled over long distances. Their effect was strong: LFP traces at any site could be predicted by the superposition of waves that were evoked by spiking in a ∼1.5-mm radius. As stimulus contrast increased, both the magnitude and the distance traveled by the waves progressively decreased. We conclude that the relative weight of feedforward and lateral inputs in visual cortex is not fixed, but rather depends on stimulus contrast. Lateral connections dominate at low contrast, when spatial integration of signals is perhaps most beneficial.
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