Spatial and temporal frequency tuning in striate cortex: Functional uniformity and specializations related to receptive field eccentricity

Department of Physiology, Monash University, Clayton VIC 3800, Australia.
European Journal of Neuroscience (Impact Factor: 3.18). 03/2010; 31(6):1043-62. DOI: 10.1111/j.1460-9568.2010.07118.x
Source: PubMed


In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3 degrees to 70 degrees eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell's optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50 degrees). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high-speed (> 30 degrees/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.

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    • "To do this, we made multi-electrode recordings from area MT of marmoset , a diurnal New World monkey in which area MT lies exposed on the cortical surface. The functional properties of neurons in the LGN (White et al. 2001; Solomon et al. 2002), V1 (Yu et al. 2010; Cheong et al. 2013), and area MT (Rosa and Elston 1998; Solomon et al. 2011) of marmoset are qualitatively and quantitatively similar to those of Old World macaque monkey. We first characterize the spatial and temporal structure of noise correlations between pairs of single neurons and show its stimulus dependence. "
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    ABSTRACT: In humans and other primates, the analysis of visual motion includes populations of neurons in the middle-temporal (MT) area of visual cortex. Motion analysis will be constrained by the structure of neural correlations in these populations. Here, we use multi-electrode arrays to measure correlations in anesthetized marmoset, a New World monkey where area MT lies exposed on the cortical surface. We measured correlations in the spike count between pairs of neurons and within populations of neurons, for moving dot fields and moving gratings. Correlations were weaker in area MT than in area V1. The magnitude of correlations in area MT diminished with distance between receptive fields, and difference in preferred direction. Correlations during presentation of moving gratings were stronger than those during presentation of moving dot fields, extended further across cortex, and were less dependent on the functional properties of neurons. Analysis of the timescales of correlation suggests presence of 2 mechanisms. A local mechanism, associated with near-synchronous spiking activity, is strongest in nearby neurons with similar direction preference and is independent of visual stimulus. A global mechanism, operating over larger spatial scales and longer timescales, is independent of direction preference and is modulated by the type of visual stimulus presented.
    Cerebral Cortex 06/2014; 25(9). DOI:10.1093/cercor/bhu111 · 8.67 Impact Factor
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    • "In the present study, the local mapping data show a restricted reorganization similar to that observed in most previous studies in which anesthetized monkeys were also used. The differences in the results could also be due to the different eccentricities of the lesions, as there is some evidences that the response properties of cells in central and peripheral V1 may be slightly different (Battaglini et al. 1993; Yu et al. 2010). An early report has also shown that the representation of the periphery may have a lesser capacity to show the topographic reorganization, particularly short-term reorganization (Rosa et al. 1995). "
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    ABSTRACT: We quantified the capacity for reorganization of the topographic representation of area V1 in adult monkeys. Bias-free automated mapping methods were used to delineate receptive fields (RFs) of an array of neuronal clusters prior to, and up to 6 h following retinal lesions. Monocular lesions caused a significant reorganization of the topographic map in this area, both inside and outside the cortical lesion projection zone (LPZ). Small flashed stimuli revealed responses up to 0.85 mm inside the boundaries of the LPZ, with RFs representing regions of undamaged retina immediately surrounding the lesion. In contrast, long moving bars that spanned the scotoma resulting from the lesion revealed responsive units up to 1.87 mm inside the LPZ, with RFs representing interpolated responses in this region. This reorganization is present immediately after monocular retinal lesioning. Both stimuli showed a similar and significant (5-fold) increase of the RF scatter in the LPZ, 0.56 mm (median), compared with the undamaged retina, 0.12 mm. Our results reveal an array of preexisting subthreshold functional connections of up to 2 mm in V1, which can be rapidly mobilized independently from the differential qualitative reorganization elicited by each stimulus.
    Cerebral Cortex 09/2012; 24(1). DOI:10.1093/cercor/bhs208 · 8.67 Impact Factor
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    • "In addition, V1 cells processing locations in peripheral vision have larger receptive fields than central ones (e.g. Hubel & Wiesel, 1974), and these cells' contrast sensitivity is biased to lower spatial frequencies (Tolhurst & Thompson, 1981; Yu et al., 2010). This presumably underlies the bias of human peripheral vision towards lower spatial frequencies compared to the fovea (Cannon, 1985; Hilz & Cavonius, 1974; Mullen & Kingdom, 2002; Peli, Yang, Goldstein, & Reeves, 1991; Pointer & Hess, 1989; Robson & Graham, 1981; Rovamo & Virsu, 1979; Wright & Johnston, 1983). "
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    ABSTRACT: We conducted suprathreshold discrimination experiments to compare how natural-scene information is processed in central and peripheral vision (16° eccentricity). Observers' ratings of the perceived magnitude of changes in naturalistic scenes were lower for peripheral than for foveal viewing, and peripheral orientation changes were rated less than peripheral colour changes. A V1-based Visual Difference Predictor model of the magnitudes of perceived foveal change was adapted to match the sinusoidal grating sensitivities of peripheral vision, but it could not explain why the ratings for changes in peripheral stimuli were so reduced. Perceived magnitude ratings for peripheral stimuli were further reduced by simultaneous presentation of flanking patches of naturalistic images, a phenomenon that could not be replicated foveally, even after M-scaling the foveal stimuli to reduce their size and the distances from the flankers. The effects of the peripheral flankers are very reminiscent of crowding phenomena demonstrated with letters or Gabor patches.
    Vision research 05/2011; 51(14):1686-98. DOI:10.1016/j.visres.2011.05.010 · 1.82 Impact Factor
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