Neuroanatomical correlates of visual field bias: A sensitive system for detecting potential threats?

Abstract

Preferred pathways of emotional processing were investigated in an fMRI study where fearful and neutral faces were presented in the left, right or central visual field. Seventeen male volunteers were imaged at 3.0 T using GE-EPI. Spatial preprocessing and statistical analyses were performed using SPM2. A preference for peripheral fearful and central neutral faces was found in frontal and temporal areas, temporal pole, putamen, and ACC. A subset showed a significant preference for fearful faces in the right hemifield. These results seem to suggest a sensitive network for preferential processing of potential threat signals.

Introduction

The concept of cerebral lateralization emerged in the second half of the 19th century, triggered by Broca's discoveries of lateralized language functions. A link between the right hemisphere and emotional processing was established as early as in the beginning of the 20th century by Mills, 1912a, Mills, 1912b. Based on neuropsychological observations in patients with unilateral brain lesions, the right hemisphere model was developed which states that the right hemisphere is dominant in emotional processing, regardless of valence (Borod et al., 1983). However, several observations, in particular on healthy subjects, did not seem to support this model. Therefore, more recent hypotheses posit that hemispheric specialisation of emotion depends on valence (Ehrlichman, 1987), on associated approach or withdrawal behaviour (Davidson et al., 1990), or reflects behavioural activation and inhibition systems (Gray and McNaughton, 2000). For a recent review of these theories see Demaree et al. (2005).

Generally, a visual-field bias in the judgment of facial expressions (Adolphs, 2001, Asthana and Mandal, 2001, Jansari, 2000) or a bias in infant holding (Vauclair and Donnot, 2005) is interpreted in terms of the hemispheric dominance theory. Images presented in the left or right visual field are assumed to be preferentially processed by the right or left hemisphere, respectively. The finding of Jansari et al. (2000) that the perceptual discrimination of emotional faces from neutral faces was better if positively valenced faces were presented to the viewer's right and negatively valenced faces were presented to the viewer's left was thus interpreted as a preference of the right and left hemisphere for negatively and positively valenced emotions, respectively. Until the 1970s, functional hemispheric specialisation was thought to be a specific human trait. However, since then cerebral asymmetry has also been found in a number of vertebrates. In animals with laterally placed eyes, e.g. birds, toads and fish, significant asymmetries in eye use have been detected, and a study in chick embryos even revealed the genetic, hormonal and experiential factors that interact to determine the lateralized organization of visual functions (see Vallortigara and Rogers, 2005 for review). Thus, it seems that hemispheric specialisation is widespread in animals and may have emerged early in evolution.

This brings up the question about the purpose of functional hemispheric specialisation of the brain. Obviously, there should be clear disadvantages for creatures with significant perceptual asymmetries because the physical world doesn't show any preference for left and right, and enemies as well as prey might approach from any side (Vallortigara and Rogers, 2005). However, possibly clear-cut advantages arise from functional specialisation. Firstly, neural capacity should be increased because specialisation of one hemisphere for a particular function leaves the other hemisphere free for different tasks. Secondly, the dominance of one hemisphere would be a convenient way of preventing simultaneous initiation of incompatible responses in organisms with laterally placed eyes (Vallortigara and Rogers, 2005). In the light of these hypothetical advantages and the above-mentioned findings in a variety of animals, it seems reasonable to assume that humans also show perceptual asymmetries, even though those were only detected in highly artificial experimental situations (i.e., tachistoscopic viewing or dichotic listening) and do not seem to play a direct role in everyday live.

The advent of neuroimaging techniques like positron emission tomography (PET), functional magnetic resonance imaging (fMRI) and electrophysiological methods like electro encephalography (EEG) and magnetic encephalography (MEG) allows to investigate these hypotheses in more detail in healthy human subjects. While the lateralization was found to be quite strict at the primary sensory level where input from the right visual field is processed in the left visual cortex and vice versa, matters are less clear for more complex cognitive functions, e.g. for language processing which was generally supposed to be a left hemispheric function, at least in right-handers (Lindell, 2006). Thus, not surprisingly, recent meta-analyses of neuroimaging studies of emotion conclude that the concept of lateralization of emotional processing cannot be supported on a hemispheric level, suggesting that functional specialisation of brain regions involved in emotional processing is rather more complex and region-specific (Murphy, 2003, Phan, 2002, Wager, 2003) than predicted by previous theories based on lesion studies and neuropsychological observations. However, functional specialisation does not necessarily require lateralization to one hemisphere. In our opinion, the observed visual field biases (Adolphs, 2001, Asthana and Mandal, 2001, Jansari, 2000, Vauclair and Donnot, 2005) suggest that there are preferred pathways for emotional contents which may also depend on the side of input.

In order to investigate the hypothesized preferred pathways in more detail we performed an fMRI study, presenting fearful and neutral faces to the left, right or central visual field. Our hypothesis is that a visual field bias in the judgment of facial expressions should be reflected in the neural substrates of emotional processing. We expected to find specific neuronal networks for emotional processing depending on the side of input and emotional content.