Chromatic and Achromatic Spatial Resolution of Local Field Potentials in Awake Cortex

Cerebral Cortex, October 2015;25: 3877–3893 doi: 10.1093/cercor/bhu270 Advance Access Publication Date: 21 November 2014 Original Article ORIGINAL ARTICLE Chromatic and Achromatic Spatial Resolution Michael Jansen1, Xiaobing Li1, Reza Lashgari1,4, Jens Kremkow1, Yulia Bereshpolova3, Harvey A. Swadlow1,3, Qasim Zaidi2, and Jose-Manuel Alonso1,3 1 Department of Biological Sciences and 2Graduate Center for Vision Research, SUNY College of Optometry, New York, NY, USA, 3Psychology, University of Connecticut, Storrs, CT, USA, and 4Department of Biomedical Engineering, School of Electrical Engineering, Iran University of Science and Technology, Tehran, Iran Address correspondence to Jose-Manuel Alonso, State University of New York, State College of Optometry, 33 West, 42nd street, 17th floor, New York, NY 10036, USA . Email: Abstract Local field potentials (LFPs) have become an important measure of neuronal population activity in the brain and could provide robust signals to guide the implant of visual cortical prosthesis in the future. However, it remains unclear whether LFPs can detect weak cortical responses (e.g., cortical responses to equiluminant color) and whether they have enough visual spatial resolution to distinguish different chromatic and achromatic stimulus patterns. By recording from awake behaving macaques in primary visual cortex, here we demonstrate that LFPs respond robustly to pure chromatic stimuli and exhibit ∼2.5 times lower spatial resolution for chromatic than achromatic stimulus patterns, a value that resembles the ratio of achromatic/chromatic resolution measured with psychophysical experiments in humans. We also show that, although the spatial resolution of LFP decays with visual eccentricity as is also the case for single neurons, LFPs have higher spatial resolution and show weaker response suppression to low spatial frequencies than spiking multiunit activity. These results indicate that LFP recordings are an excellent approach to measure spatial resolution from local populations of neurons in visual cortex including those responsive to color. Key words: LFP, area V1, color, receptive field, striate cortex Introduction The primary visual cortex (area V1) is fed by 3 major thalamic pathways that carry different combinations of inputs from cone photoreceptors that are sensitive to long (L), medium (M), and short (S) wavelengths. Parvocellular neurons compute the difference between L and M inputs, koniocellular neurons the difference between S and the sum of L + M inputs, and magnocellular neurons compute L + M sums (Derrington et al. 1984; Sun et al. 2006). Magnocellular and parvocellular neurons measure local contrast by taking the difference between inputs to their receptive field centers and surrounds (Wiesel and Hubel 1966; Reid and Shapley 1992, 2002; Lee et al. 1998). When the center and surround involve the same cone combination, the subtraction generates band-pass spatial frequency tuning, as is the case in magnocellular neurons, where only a band of intermediate spatial frequencies pass to later stages of visual processing (Hicks et al. 1983; Derrington and Lennie 1984). Conversely, when the center-surround subtraction involves different cones, as in the parvocellular pathway, the neurons only pass the low spatial © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact of Local Field Potentials in Awake Cortex 3878 | Cerebral Cortex, 2015, Vol. 25, No. 10 Materials and Methods Visual Stimuli Stimuli were presented on a cathode ray tube (CRT) monitor (Sony GDM F520, refresh rate: 160 Hz). The receptive field of the LFP was mapped with sparse noise consisting of either 256 light squares presented on a 16 × 16 grid (0.71°/square side) or 1600 light squares presented on a 40 × 40 grid (0.59°/square side). Light squares were flashed for 20 ms and separated by 100 ms. When a single neuron was recorded simultaneously with the LFP, the grating stimulus was centered at the receptive field position of the neuron. In these cases, the receptive field center of each single neuron was mapped using the spike-triggered average of Hartley stimuli (Ringach et al. 1997) presented at 80 Hz. The Hartley stimuli were made of gratings with 88 different orientations, 41 different spatial frequencies, and 4 different phases, usually presented at 2–3 different sizes (0.1, 0.2, and 0.4° per pixel). In LFP recordings, the spatial frequency tuning was measured with large grating stimuli of 8° diameter and 0° orientation. We chose these stimulus parameters because equiluminant chromatic gratings generated the most robust LFP response transients to large gratings (see Results for size tuning in this article) and the amplitude of the LFP transient was poorly tuned to orientation (Lashgari et al. 2012). LFPs are also untuned to orientation when flashed bars are used (Mineault et al. 2013). The emission spectra for the red (R), green (G), and blue (B) monitor phosphors were measured with a Photo Research PR 650 SpectraScan spectroradiometer. Since our LFP recordings cover foveal receptors, excitations for the long- (L), medium(M), and short- (S) wavelength sensitive cones were obtained for the 3 phosphors from the dot product of the emission spectra and the Smith–Pokorny 2° cone fundamentals (Smith and Pokorny 1975). Using the procedure described by Zaidi and Halevy (1993), this cone response space was converted to the cardinal color space used by Derrington et al. (1984) defined by (L − M), (S), and (L + M + S) axes. For simplicity, we will call (L − M) the red/green axis (RG), S the blue/yellow axis (BY), and (L + M + S) the light/dark or luminance axis (LD). S and (L + M) cone absorptions are constant in the RG axis, L and M are constant in the BY axis, and all cone absorptions vary together in the LD axis. Figure 1 shows the L, M, and S coordinates at the intersection and ends of the 3 cardinal axes. Cone contrasts were calculated for each axis as in the following equation: Surgery and Preparation Two adult male rhesus monkeys were surgically implanted with a head post, a scleral eye coil, and a recording chamber. Inside the recording chamber, we implanted a chronic multielectrode array with 3–7 independently movable electrodes to record LFP activity (Swadlow et al. 2005). The electrodes were 40-µm-diameter platinum–tungsten filaments, pulled, and sharpened to a fine tip of ∼1 µm. Animals were trained to hold a bar and fixate on a small cross of 0.12°. After fixating for 0.5 s, static sine-wave gratings were presented over a period of 2 s to measure the chromatic selectivity, spatial frequency tuning, and size tuning of LFPs. Each (...truncated)