Mapping the complex topological organization of the human parietal face area

Abstract

The macaque monkey ventral intraparietal area (VIP) contains neurons with aligned visual-tactile receptive fields anchored to the face and upper body. Our previous fMRI studies using standard head coils found a human parietal face area (VIP+ complex; putative macaque VIP homologue) containing superimposed topological maps of the face and near-face visual space. Here, we construct high signal-to-noise surface coils and used phase-encoded air puffs and looming stimuli to map topological organization of the parietal face area at higher resolution. This area is consistently identified as a region extending between the superior postcentral sulcus and the upper bank of the anterior intraparietal sulcus (IPS), avoiding the fundus of IPS. Using smaller voxel sizes, our surface coils picked up strong fMRI signals in response to tactile and visual stimuli. By analyzing tactile and visual maps in our current and previous studies, we constructed a set of topological models illustrating commonalities and differences in map organization across subjects. The most consistent topological feature of the VIP+ complex is a central-anterior upper face (and upper visual field) representation adjoined by lower face (and lower visual field) representations ventrally (laterally) and/or dorsally (medially), potentially forming two subdivisions VIPv (ventral) and VIPd (dorsal). The lower visual field representations typically extend laterally into the anterior IPS to adjoin human area AIP, and medially to overlap with the parietal body areas at the superior parietal ridge. Significant individual variations are then illustrated to provide an accurate and comprehensive view of the topological organization of the parietal face area.

Spatiotemporal integration of looming visual and tactile stimuli near the face

“…An sROI located at the confluence of the postcentral sulcus and anterior intraparietal sulcus was outlined and labeled VIP+ (plus sign indicates a complex with multiple subdivisions; Huang et al, ; Sereno & Huang, ). Both LH‐VIP+ and RH‐VIP+ showed higher F Q3 in response to contralateral stimuli than ipsilateral stimuli in all event types except TVoS (LH) (Figure ).…”

“…(3) spatial congruency (Macaluso & Driver, 2001, 2005 or precise alignment of receptive fields across modalities (Avillac et al, 2005(Avillac et al, , 2007Dong et al, 1994;Duhamel et al, 1998;Graziano et al, 1994Graziano et al, , 1997Huang et al, 2017;Ishida et al, 2010;McCollum et al, 2012;; (4) directional congruency across modalities (e.g., looming or receding; Maier, Neuhoff, Logothetis, & Ghazanfar, 2004;Maier et al, 2008;Tyll et al, 2013); and (5) temporal synchrony across modalities (Avillac et al, 2007;Bushara, Grafman, & Hallett, 2001;Bushara et al, 2003;Calvert et al, 2001;Marchant et al, 2012). In the present study, spatially aligned and directionally congruent looming visual and tactile stimuli were delivered to either side of the face with a varying temporal offset in psychophysical and fMRI experiments.…”

“…Previous neurophysiological and neuroimaging studies on multisensory integration have considered the following factors in designing their experiments and stimuli: (1) stimulus modalities (visual, auditory, tactile, and so on); (2) semantic or content congruency across modalities (Beauchamp, ; Beauchamp et al, , 2004b; Calvert, ); (3) spatial congruency (Macaluso & Driver, 2001, 2005) or precise alignment of receptive fields across modalities (Avillac et al, 2005, ; Dong et al, ; Duhamel et al, ; Graziano et al, 1994, ; Huang et al, ; Ishida et al, ; McCollum et al, ; Sereno & Huang, 2006); (4) directional congruency across modalities (e.g., looming or receding; Maier, Neuhoff, Logothetis, & Ghazanfar, 2004; Maier et al, ; Tyll et al, ); and (5) temporal synchrony across modalities (Avillac et al, ; Bushara, Grafman, & Hallett, 2001; Bushara et al, ; Calvert et al, ; Marchant et al, ). In the present study, spatially aligned and directionally congruent looming visual and tactile stimuli were delivered to either side of the face with a varying temporal offset in psychophysical and fMRI experiments.…”

“…We designed and constructed a multisensory apparatus to deliver spatially aligned looming visual and tactile stimuli near the face in psychophysical and fMRI experiments (Figure ). Visual stimuli (looming balls) were simulated in a virtual reality environment written in the C language using the OpenGL Performer library (Huang et al, ; Huang, Chen, & Sereno, ; Huang et al, ), and rendered at a resolution of 1,024 × 768 pixels with a refresh rate of 60 Hz on a two‐dimensional (2D) CRT monitor (psychophysical experiment) or on an LCD projector (fMRI experiment). Tactile stimuli (100‐ms air puffs; 50–55 psi at air cylinder output) were delivered tangentially to either side of the face via a flexible hose (1/4‐in.…”

“…Monkey neurophysiological and human neuroimaging studies have revealed multiple cortical areas playing important roles in multisensory integration: (1) middle temporal complex (MT+), including the medial superior temporal area (MST) (Beauchamp, Yasar, Kishan, & Ro, ; Blake, Sobel, & James, ; Hagen et al, ); (2) superior temporal sulcus (STS) (Beauchamp, Argall, Bodurka, Duyn, & Martin, ; Beauchamp, Lee, Argall, & Martin, ; Beauchamp, Yasar, Frye, & Ro, ; Calvert, ; Calvert, Hansen, Iversen, & Brammer, ; Maier, Chandrasekaran, & Ghazanfar, ; Marchant, Ruff, & Driver, ; Seifritz et al, ; Tyll et al, ); (3) ventral intraparietal area (VIP) (Avillac, Deneve, Olivier, Pouget, & Duhamel, ; Avillac, Ben Hamed, & Duhamel, ; Bremmer et al, ; Colby, Duhamel, & Goldberg, ; Duhamel, Colby, & Goldberg, ; Huang, Chen, Tran, Holstein, & Sereno, ; Huang, Chen, & Sereno, ; Ishida, Nakajima, Inase, & Murata, ; McCollum, Klam, & Graf, ; Sereno & Huang, ); (4) precentral polysensory zone (PZ) and ventral premotor cortex (PMv) (Bremmer et al, ; Fogassi et al, ; Graziano & Gandhi, ; Graziano, Yap, & Gross, ; Graziano, Hu, & Gross, ; Huang & Sereno, ); and (5) area 7b at the posterior lateral sulcus (Dong, Chudler, Sugiyama, Roberts, & Hayashi, ; Graziano, Gross, Taylor, & Moore, ; Ishida et al, ). Most of these multisensory areas also respond to visual, auditory, and/or tactile motion, including looming stimuli.…”