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. 2013 Nov 27;33(48):18740-5.
doi: 10.1523/JNEUROSCI.3923-13.2013.

Motion-sensitive responses in visual area V4 in the absence of primary visual cortex

Michael C Schmid  1 , Joscha T Schmiedt, Andrew J Peters, Richard C Saunders, Alexander Maier, David A Leopold
Affiliations

Motion-sensitive responses in visual area V4 in the absence of primary visual cortex

Michael C Schmid et al. J Neurosci. .

Abstract

Neurons in cortical ventral-stream area V4 are thought to contribute to important aspects of visual processing by integrating information from primary visual cortex (V1). However, how V4 neurons respond to visual stimulation after V1 injury remains unclear: While electrophysiological investigation of V4 neurons during reversible V1 inactivation suggests that virtually all responses are eliminated (Girard et al., 1991), fMRI in humans and monkeys with permanent lesions shows reliable V1-independent activity (Baseler et al., 1999; Goebel et al., 2001; Schmid et al., 2010). To resolve this apparent discrepancy, we longitudinally assessed neuronal functions of macaque area V4 using chronically implanted electrode arrays before and after creating a permanent aspiration lesion in V1. During the month after lesioning, we observed weak yet significant spiking activity in response to stimuli presented to the lesion-affected part of the visual field. These V1-independent responses showed sensitivity for motion and likely reflect the effect of V1-bypassing geniculate input into extrastriate areas.

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Figures

Figure 1.
Figure 1.
Longitudinal investigation of V4 neuronal responses before and after V1 lesion. A, fMRI-based retinotopic map of visual cortex for Monkey B, acquired before lesioning V1 using alternating rotating checkerboard wedges. B, The lesion was targeted to eliminate the V1 representation of the right horizontal meridian between ∼2–7° of visual eccentricities (red) while leaving lower vertical meridian representation intact (blue). C, Stimuli close to the right horizontal meridian inside the lesion-affected visual space are labeled “scotoma stimuli” and stimuli close to the vertical meridian are labeled “control stimuli.” D, Coronal section of V1 for Monkey B (left) and F (right). Scale bars, 5 mm.
Figure 2.
Figure 2.
V4 responses to scotoma stimuli are severely degraded but not abolished. A, Detection performance of Monkey B in a perimetry task at various stimulus positions in the lower right visual field during the week before (left, n = 532 trials from 2 sessions) and after (right, n = 705 trials from 3 sessions) the V1 lesion. Dashed magenta line indicates scotoma border estimate. B, V4 MUA array RF of Monkey B before (left, n = 3524 trials from n = 5 sessions) and after (right, n = 4882 trials from n = 7 sessions) V1 lesion (n = 53 electrodes). Black dots indicate RF centers of individual electrodes. C, Detection performance as in A for Monkey F before (n = 1344 trials from 3 sessions) and after V1 lesion (n = 206 trials from 1 session). D, V4 array RF as in B for Monkey F (n = 47 electrodes, n = 2193 and 4530 trials from n = 3 and 6 sessions from before and after V1 lesion, respectively). White dot indicates RF center of example electrode shown in E. E, MUA response from example electrode with large RF coverage in Monkey F to stimuli close to vertical meridian (left, x = 0 to 1°, y = −3 to −4°) and horizontal meridian (right, x = 3 to 4°, y = −2 to 0°) before and after V1 lesion. Shading indicates SEM. F, Distribution of MUA responses to stimuli close to vertical meridian (left) and horizontal meridian (right). Each dot indicates the average MUA response of a recording site before and after V1 lesion. Color shading indicates p value of postlesion responses (Wilcoxon signed rank test compared with prestimulus period). Solid gray lines indicate identical prelesion and postlesion responses. ecc., Eccentricity.
Figure 3.
Figure 3.
V4 MUA responses to scotoma stimuli show sensitivity for motion. A, B, Example MUA time courses for moving (blue) and static (green) gratings before (left) and after (right) V1 lesion from Monkey B (A) and Monkey F (B). C, Distribution of responses to moving and static gratings of all recording sites for scotoma (top row) and control (bottom row) stimuli. Each dot represents the average MUA response of a recording site, before the lesion (black symbols, left column; Monkey B: n = 7 sessions; Monkey F: n = 4 sessions) or after (red symbols, right column; Monkey B: n = 3 sessions, 5–9 d after lesion; Monkey F: n = 5 sessions, 9–18 d after lesion). Insets, Magnified view of the gray box.
Figure 4.
Figure 4.
V1-independent tuning for direction of motion in V4. A, MUA time courses (left column) and tuning profile (right column) from example sessions before (top row) and after (bottom row) V1 lesion of Monkey F. Tuning is quantified by taking the d′ value between the maximum (blue) and minimum (green) MUA response. Error bars indicate SEM. B, Smoothed histograms of d′ values for direction of motion tuning from all responsive recording sites and sessions before (gray, Monkey B: n = 5 sessions, Monkey F: n = 3 sessions) and after (red, Monkey B: n = 4 sessions, Monkey F: n = 11 sessions) the V1 lesion for scotoma or control stimuli. Larger symbols indicate mean values. n.s. indicates a difference not significant at p < 0.05 (Mann–Whitney U test).
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