Retinotopic and Lateralized Processing of Spatial Frequencies in Human Visual Cortex during Scene Categorization

Abstract

Using large natural scenes filtered in spatial frequencies, we aimed to demonstrate that spatial frequency processing could not only be retinotopically mapped but could also be lateralized in both hemispheres. For this purpose, participants performed a categorization task using large black and white photographs of natural scenes (indoors vs. outdoors, with a visual angle of 24° × 18°) filtered in low spatial frequencies (LSF), high spatial frequencies (HSF), and nonfiltered scenes, in block-designed fMRI recording sessions. At the group level, the comparison between the spatial frequency content of scenes revealed first that, compared with HSF, LSF scene categorization elicited activation in the anterior half of the calcarine fissures linked to the peripheral visual field, whereas, compared with LSF, HSF scene categorization elicited activation in the posterior part of the occipital lobes, which are linked to the fovea, according to the retinotopic property of visual areas. At the individual level, functional activations projected on retinotopic maps revealed that LSF processing was mapped in the anterior part of V1, whereas HSF processing was mapped in the posterior and ventral part of V2, V3, and V4. Moreover, at the group level, direct interhemispheric comparisons performed on the same fMRI data highlighted a right-sided occipito-temporal predominance for LSF processing and a left-sided temporal cortex predominance for HSF processing, in accordance with hemispheric specialization theories. By using suitable method of analysis on the same data, our results enabled us to demonstrate for the first time that spatial frequencies processing is mapped retinotopically and lateralized in human occipital cortex.

Effective connectivity in the neural network underlying coarse-to-fine categorization of visual scenes. A dynamic causal modeling study

“…It is important to note that since the DCM analysis was performed on regions of the right hemisphere, as did Kveraga et al (2007), the inferred effective connectivity in our study may primarily apply to the right hemisphere. Besides, to our knowledge, there is no evidence of a symmetric connectivity network between the right and the left hemisphere and previous studies have shown right hemisphere predominance for coarse-to-fine analysis (Musel et al, 2013;Peyrin, Baciu, Segebarth, & Marendaz, 2004;Peyrin, Chauvin, Chokron, & Marendaz, 2003;Peyrin et al, 2005).…”

“…Our fMRI results revealed that coarse-to-fine sequences (compared to fine-to-coarse sequences) elicited stronger bilateral activation in three cortical hubs: the occipital cortex (C), the inferior frontal gyrus (IFG), and the fusiform and parahippocampal gyri (FG). The involvement of the occipital cortex in visual perception and in spatial frequency processing has already been well-established using sinusoidal gratings (Henriksson, Nurminen, & Vanni, 2008;Sasaki et al, 2001) and scenes (Musel et al, 2013). Activation in the left inferior frontal gyrus (peak coordinates x, y, z: À36, 16, À10) almost overlaps with the orbitofrontal activation reported by Bar et al (2006;x, y, z: À36, 23, À14) and Kveraga et al (2007;x, y, z: À30, 28, À11).…”

The neural bases of spatial frequency processing during scene perception

“…Cerebral asymmetries have been observed in behavioral studies conducted on healthy participants (Sergent, 1982, 1983; Sergent and Hellige, 1986; Kitterle et al, 1990, 1992; Chokron et al, 2003; Peyrin et al, 2003), in neurological patients (Robertson et al, 1988; Lamb et al, 1990; Robertson and Lamb, 1991; Peyrin et al, 2006; Dos Santos et al, 2013), and from functional neuroimaging studies (Fink et al, 1996, 2000; Martinez et al, 1997, 2001; Heinze et al, 1998; Kenemans et al, 2000; Mangun et al, 2000; Yamaguchi et al, 2000; Wilkinson et al, 2001; Han et al, 2002; Iidaka et al, 2004; Lux et al, 2004; Peyrin et al, 2004; Weissman and Woldorff, 2005; Musel et al, 2013). However, the hemispheric specialization for spatial frequency processing was largely inferred from studies assessing cerebral asymmetries during the processing of global and local information.…”

“…Images from the second set are “flipped” by 180° in the midsagital plane, thus providing “mirror” images of the first set. Contrasts between “unflipped” and “left-right flipped” functional volumes from the same experimental condition allow to compare activity in one hemisphere with activity in homologous regions of the other hemisphere (Iidaka et al, 2004; Peyrin et al, 2004, 2005; Musel et al, 2013; see also Cousin et al, 2006 for an application of this method on language processes; Figure 3 ). This method revealed greater activation in the right than the left middle occipital gyrus for LSF scene recognition, and greater activation in the left than the right middle occipital gyrus for HSF scene recognition ( Figure 2B ).…”

“…While some studies have clearly demonstrated that attentional processes exert control on hemispheric specialization in the processing of global and local information at high-level stages of visual processing (e.g., via the temporo-parietal junction; Robertson et al, 1988; Robertson and Lamb, 1991; Fink et al, 1996; Heinze et al, 1998; Yamaguchi et al, 2000; Wilkinson et al, 2001; Weissman and Woldorff, 2005), other studies have evidenced hemispheric asymmetries at lower-level stages, in the occipital cortex (Fink et al, 1997, 2000; Peyrin et al, 2004; Musel et al, 2013). However, activation of the occipital cortex was frequently associated with activation of the temporo-parietal junction in these studies.…”