Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture

Abstract

Visual attention can be driven by the affective significance of visual stimuli before full-fledged processing of the stimuli. Two kinds of models have been proposed to explain this phenomenon: models involving sequential processing along the ventral visual stream, with secondary feedback from emotion-related structures ("two-stage models"); and models including additional short-cut pathways directly reaching the emotion-related structures ("two-pathway models"). We tested which type of model would best predict real magnetoencephalographic responses in subjects presented with arousing visual stimuli, using realistic models of large-scale cerebral architecture and neural biophysics. The results strongly support a "two-pathway" hypothesis. Both standard models including the retinotectal pathway and nonstandard models including cortical-cortical long-range fasciculi appear plausible.

Prefrontal-Occipitoparietal Coupling Underlies Late Latency Human Neuronal Responses to Emotion

“…It should be noted that the late latency response we report is in contrast to early emotion-evoked neuromagnetic activity observed in ventral extrastriate cortex (Rudrauf et al, 2008) beginning from 0.1 s poststimulus onset. We do, however, observe, at the sensor level an emotional modulation of the ERFs before the onset of mLPP time window at 0.2-0.4 s (Fig.…”

Brain mechanisms for emotional influences on perception and attention: What is magic and what is not

“…Some techniques might improve these investigations, as shown by a recent fMRI study using a fast slice acquisition protocol (Sabatinelli, et al, 2009) that confirmed a sequential two-stage activation from amygdala to fusiform cortex. Thus, this study could show that a differential emotional discrimination arose in the amygdala approximately 1 s before extrastriate occipital cortex (no differential effect was found in the striate cortex), consistent with a re-entrant organization of emotional inputs along visual pathways (Vuilleumier, 2005;Rudrauf, et al, 2008;Sabatinelli, et al, 2009). However, this timing difference is relatively long and somewhat hard to reconcile with responses latencies observed with other techniques (single neuron firing rate, EEG or MEG), and even fast fMRI might not have sufficient temporal resolution to establish a precise timing of information transmission.…”

“…In addition, recent DTI data in humans suggest that early occipital areas may project to anterior temporal lobe (including amygdala) through direct white-matter fibers in the inferior longitudinal fasciculus (Catani, et al, 2003;Gschwind, et al, in press). Moreover, MEG recordings and connectivity models of brain responses to visual emotional stimuli suggest that the latency and distribution of activity in occipitotemporal regions is best accounted for by a functional architecture involving both rapid inputs through a short-cut to the amygdala and subsequent feedback from amygdala to early cortical areas, rather than by a strictly sequential processing along the ventral visual stream (Rudrauf, et al, 2008). These results support a dual route hypothesis, but a subcortical route or cortico-cortical long-range pathways appear equally plausible, and the exact anatomical substrates of these effects therefore remain to be clarified.…”

“…Other imaging methods (such as arterial spin labeling or positron emission tomography) might also be usefully exploited to investigate changes in baseline activity that are potentially induced by anxiety, task difficulty, or higher error rates, but typically cancelled out in standard contrast with BOLD fMRI. Conversely, EEG and MEG studies can provide valuable information regarding the time-course of emotion-related and attention-related effects (Pourtois, et al, 2004;Pourtois, Thut, et al, 2005;Keil, et al, 2005;Luo, et al, 2010;Rudrauf, et al, 2008), but the anatomical sites of the effects remain difficult to establish with certainty even if sophisticated mathematical models can yield precious information on neural sources (e.g. Pourtois, Thut, et al, 2005).…”

See it with feeling: affective predictions during object perception

“…Some researchers argue for a subcortical route by which low spatial frequency visual information about objects and faces can bypass V1 via the amygdala to represent affective value in the body and behaviour (e.g. LeDoux 1996LeDoux , 2000Weiskrantz 1996;Morris et al 1998;Catani et al 2003;Rudrauf et al 2008), whereas others argue that such a circuit is not functional in primates (Rolls 2000;Pessoa & Ungerleider 2004). Either way, affective predictions do not necessarily require a purely subcortical route.…”