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

Abstract

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.

Active Vision in Marmosets: A Model System for Visual Neuroscience

“…They have been used in the study of auditory and vocal processing in the awake and behaving conditions for over a decade (Lu et al, 2001a,b;Barbour and Wang, 2003;Bendor and Wang, 2005;Wang et al, 2005;Eliades and Wang, 2008a,b) and necessary techniques for their handling and behavioral conditioning for auditory tasks have been established (Osmanski and Wang, 2011;Remington et al, 2012). The anatomy and physiology of the marmoset visual systems have been examined in detail for anesthetized animals (Kaas et al, 1978;Huerta et al, 1986;Krubitzer and Kaas, 1990;Tweedale, 2000, 2005;Solomon et al, 2002;Collins et al, 2005;Roe et al, 2005;Szmajda et al, 2005;Rosa et al, 2009;Yu et al, 2010;Martin et al, 2011;Solomon et al, 2011;Valverde Salzmann et al, 2012;Chaplin et al, 2013), including a stereotaxic atlas of the marmoset brain (Paxinos et al, 2012), and recently noninvasive techniques for anatomical and functional imaging have been established (Belcher et al, 2013;Liu et al, 2013;Papoti et al, 2013), thus providing a sound basis for continued study with invasive techniques in the awake, behaving animal. One key advantage of the marmoset compared with the macaque is its lissencephalic (flat) cortex.…”

A simpler primate brain: the visual system of the marmoset monkey

“…1.1 cycles/degree within 5° of the fovea, and 0.14 cycles/degree at eccentricities beyond 50° (Sengpiel et al, 1996; Forte et al, 2005; Yu et al, 2010). At least for receptive fields in parafoveal visual space, the peak spatial frequency of V1 cells is comparable to that of marmoset LGN cells (Forte et al, 2005) and is about half that in macaque V1 (Foster et al, 1985), as expected from the smaller eye of the marmoset.…”

“…This may be different from the case in the macaque, where speed sensitivity in the corresponding region of V1 is apparent in a subpopulation of complex cells (Priebe et al, 2006). The proportion of neurons showing speed sensitivity increases in the peripheral visual field representation of marmoset V1 (Yu et al, 2010). …”

Cortical Connections of Area V6Av in the Macaque: A Visual-Input Node to the Eye/Hand Coordination System

“…However, little is known about the response properties of cells in the peripheral representation of this area. As in V1 (Yu et al, 2010), it is possible that the response properties change as a function of eccentricity, with cells subserving peripheral vision emphasizing parameters that are relevant for motion and spatial analyses. Previous studies have demonstrated that V4 appears to be an important source of visual information for occipitoparietal areas within the dorsal processing stream, including PO Ungerleider et al, 2008).…”