Primary visual cortex: awareness and blindsight

Abstract

The primary visual cortex (V1) is the principal telencephalic recipient of visual input in humans and monkeys. It is unique among cortical areas in that its destruction results in chronic blindness. However, certain patients with V1 damage, though lacking visual awareness, exhibit visually guided behavior: blindsight. This phenomenon, together with evidence from electrophysiological, neuroimaging, and psychophysical experiments, has led to speculation that V1 activity has a special or direct role in generating conscious perception. To explore this issue, this article reviews experiments that have used two powerful paradigms--stimulus-induced perceptual suppression and chronic V1 ablation--each of which disrupts the ability to perceive salient visual stimuli. Focus is placed on recent neurophysiological, behavioral, and functional imaging studies from the nonhuman primate that shed light on V1's role in conscious awareness. In addition, anatomical pathways that relay visual information to the cortex during normal vision and in blindsight are reviewed. Although the critical role of V1 in primate vision follows naturally from its position as a bottleneck of visual signals, little evidence supports its direct contribution to visual awareness.

Figure 1

Paradigms to study unconscious vision in monkeys. (a) During perceptual suppression a target stimulus is continuously presented on a video monitor, but disappears because of a visual illusion. Depicted here is generalized flash suppression (Wilke et al, 2003), where the presentation of a bright red patch at time t₁ is followed by the appearance of dynamic surrounding white dots at time t₂, causing the red patch to perceptually disappear for up to several seconds. (b) Cortical blindness following V1 lesion leads to the inability to perceive stimuli in an entire region of visual space corresponding to the retinotopic position of the lesion. Following such lesions, blindsight allows for some residual visual responses to stimuli presented to the scotoma (blind portion of the visual field).

Figure 2

Sensory and spontaneous physiology across V1 layers. (a) The basic pathways projecting from the LGN to the different layers of V1, including the magnocellular (M), parvocellular (P) and koniocellular (K). (b) Current source density (CSD) response to flashed stimuli in V1. The horizontal line is drawn through the initial current sink in layer 4C (Maier et al., 2011). (c) Spontaneous spiking responses in different cortical layers of monkeys sitting in a dark room (Snodderly and Gur, 1995). (d) Sustained CSD power that persist in the infragranular layers during the presentation of a simple stimulus (Maier et al., 2011). (e) Pattern of coherence of spontaneous high-frequency (gamma) local field potential (LFP) activity. Pairwise coherence is computed between a reference position (arrows) and all other laminar positions (Maier et al., 2010).

Figure 3

Neural correlates of perceptual suppression in V1. (a) Spiking modulation in V1 and V4 of visual responses associated with perceptual suppression vs. physical removal of a stimulus (Wilke et al., 2006). (b) Local field potential (LFP) modulation in V1 associated with perceptual suppression vs. physical removal of a stimulus (Maier et al., 2008). (c) Comparison of the effects of perceptual suppression on the blood oxygenation level-dependent (BOLD) vs. spiking signals in V1 (Maier et al., 2008).

Figure 4

Visual pathways through the dorsal thalamus to the cortex. (a) Targets of retinal ganglion cells in the diencephalon and mesencephalon. Projections are depicted on an embryonic brain to emphasize the relative positions of the retinal projection targets with respect to the neuraxis. Note that this depiction is for schematic purposes only, as the neural connections have not been formed at this stage of development. The strongest projections are to the lateral geniculate nucleus, followed by the superficial layers of the superior colliculus. (b) Schematic illustration of pathways to the cortex. There are two direct pathways from the retina to the dorsal thalamus, a retinogeniculate pathway (1) and a retinopulvinar pathway (2), along with two indirect pathways that pass through the midbrain, the retinocolliculogeniculate pathway (3) and the retinocolliculopulvinar pathway (4). Both the inferior pulvinar and the lateral geniculate nucleus project to both V1 and extrastriate visual cortex (A-D), with the former projecting predominantly to V1 (A) and the latter projecting predominantly to the extrastriate cortex (D). Of particular interest for undertanding blindsight are the direct extrastriate projections, (C) and (D). DT, dorsal thalamus; H, hypothalamus; P, pons; LGN, lateral geniculate nucleus; M, medulla oblongata; Pim, medial division of the inferior pulvinar; PT, pretectum; SC, superior colliculus; VC, visual cortex.

Figure 5

Extrastriate visual activation following V1 lesion and LGN inactivation. (a) Residual responses of single-units in multiple extrastriate visual areas following the destruction or cooling of V1 in the macaque (Bullier et al., 1994) (b) Functional magnetic resonance imaging (fMRI) responses in a range of extrastriate cortical areas in a normal hemisphere (blue), following V1 damage (red), and following V1 damage combined with acute inactivation of the LGN (green) (Schmid et al., 2010).