When seeing outweighs feeling: a role for prefrontal cortex in passive control of negative affect in blindsight

Abstract

Affective neuroscience has been strongly influenced by the view that a 'feeling' is the perception of somatic changes and has consequently often neglected the neural mechanisms that underlie the integration of somatic and other information in affective experience. Here, we investigate affective processing by means of functional magnetic resonance imaging in nine cortically blind patients. In these patients, unilateral postgeniculate lesions prevent primary cortical visual processing in part of the visual field which, as a result, becomes subjectively blind. Residual subcortical processing of visual information, however, is assumed to occur in the entire visual field. As we have reported earlier, these patients show significant startle reflex potentiation when a threat-related visual stimulus is shown in their blind visual field. Critically, this was associated with an increase of brain activity in somatosensory-related areas, and an increase in experienced negative affect. Here, we investigated the patients' response when the visual stimulus was shown in the sighted visual field, that is, when it was visible and cortically processed. Despite the fact that startle reflex potentiation was similar in the blind and sighted visual field, patients reported significantly less negative affect during stimulation of the sighted visual field. In other words, when the visual stimulus was visible and received full cortical processing, the patients' phenomenal experience of affect did not closely reflect somatic changes. This decoupling of phenomenal affective experience and somatic changes was associated with an increase of activity in the left ventrolateral prefrontal cortex and a decrease of affect-related somatosensory activity. Moreover, patients who showed stronger left ventrolateral prefrontal cortex activity tended to show a stronger decrease of affect-related somatosensory activity. Our findings show that similar affective somatic changes can be associated with different phenomenal experiences of affect, depending on the depth of cortical processing. They are in line with a model in which the left ventrolateral prefrontal cortex is a relay station that integrates information about subcortically triggered somatic responses and information resulting from in-depth cortical stimulus processing. Tentatively, we suggest that the observed decoupling of somatic responses and experienced affect, and the reduction of negative phenomenal experience, can be explained by a left ventrolateral prefrontal cortex-mediated inhibition of affect-related somatosensory activity.

Figure 1

Anatomical sections (Patients 1–4 with infarction of the primary visual cortex) or fractional diffusion anisotropy maps (Patients 5–9 with lesions affecting the optic radiation) showing the lesion of each patient. Arrows indicate lesions. Left is left.

Figure 2

Experimental design. The visual stimulus (a grey-scale male face) was presented in the SVF and BVF of nine cortically blind patients (first/second row). In habituation runs, which served as a baseline, the visual stimulus was always shown alone. In pairing runs, half of the visual stimulus presentations ended with an unpleasant human scream (third row). Each patient participated in two habituation runs and four pairing runs (only one of each is shown).

Figure 3

Startle reflex potentiation and self-reported negative affect during stimulation of the BVF and SVF. Negative affect values indicate more negative affect. Responses during pairing runs are subtracted with responses during habituation runs. Error bars represent standard errors of the mean. The asterisk indicates a significant difference between stimulation of the SVF and the BVF.

Figure 4

(A) Random effects statistical parametric map (SPM) showing a significantly stronger increase of BOLD activity during stimulation of the SVF than during stimulation of the BVF in the left VLPFC. The SPM is thresholded at a voxel-wise probability of false positives of P = 0.0001 and an extent threshold of five contiguous voxels (corresponding to P < 0.05 corrected for multiple comparison across the whole volume), and shown as surface projection and superimposed on coronal and axial sections of a standard brain (left is left). (B) Bar charts showing VLPFC and affect-related somatosensory activity during stimulation of the SVF and BVF. All responses during pairing runs are subtracted with responses during habituation runs. Affect-related somatosensory activity was extracted from the most significantly activated voxel in a region that showed significant pairing-induced activity during blind field stimulation (indicated by the red circle in A, MNI coordinates x = –42, y = –42, z = 45; Anders et al., 2004a). Error bars represent standard errors of the mean.

Figure 5

(A) Relation between subcortically triggered startle potentiation and VLPFC activity during stimulation of the BVF (r = 0.84, P = 0.04) and SVF (r = 0.90, P = 0.02). (B) Relation between VLPFC activity and affect-related somatosensory activity (r = –0.54, P = 0.08). All responses during pairing are subtracted with responses during habituation runs.

Figure 6

A model incorporating the observed relations between affective somatic changes (startle reflex potentiation), VLPFC activity, and affect-related somatosensory activity in SII during stimulation of the BVF and SVF. During stimulation of the BVF, affect-related somatic responses are associated with an increase of activity in SII and reports of negative affective experience (left). During stimulation of the SVF, additional stimulus information resulting from in-depth cortical processing is available, and VLPFC sensitivity to somatic responses increases. Increased VLPFC activity, in turn, attenuates somatosensory-related activity. We suggest that this reduction of affect-related somatosensory activity leads to a decoupling of somatic changes and experienced affect and a reduction of negative phenomenal experience (right).