How Diagnostic are Spatial Frequencies for Fear Recognition

How Diagnostic are Spatial Frequencies for Fear Recognition? Martial Mermillod Nathalie Guyader Psychology and NeuroCognition Laboratory CNRS UMR 5105 University Pierre Mendes France (martial.mermillod@upmf-grenoble.fr) Psychology and NeuroCognition Laboratory CNRS UMR 5105 University Pierre Mendes France (nguyader@yahoo.fr) Patrik Vuilleumier David Alleysson Christian Marendaz Laboratory of Neurology and Imaging of Cognition University of Geneva (patrik.vuilleumier@medecine.unige.ch) Psychology and NeuroCognition Laboratory CNRS UMR 5105 University Pierre Mendes France (David.Alleysson@upmf-grenoble.fr Christian.Marendaz@upmf-grenoble.fr) Abstract Vuilleumier, Armony, Driver & Dolan (2003) have shown that amygdala cells to fearful expressions of human faces seem to be more activated by intact or low spatial frequency (LSF) faces than high spatial frequency (HSF) faces. These fMRI results may suggest that LSF components might be processed by a subcortical pathway that is assumed to bypass the striate cortex in order to process LSF components faster than HSF components of visual stimuli. The purpose of the present paper is to test the usefulness of LSF information as compared to HSF information in a visual classification task performed by an artificial neural network and a statistical classifier. Our results show that visual information, conveyed by LSF faces, allows the statistical and connectionist models to better recognize or categorize fearful faces amongst neutral faces than HSF faces. These results suggest that high-speed connections from the magnocellular layers to the amygdala might be a fast and efficient way to perform classification of human faces with respect to their emotional expressions. Introduction Neuropsychological results have shown “blindsight” for fearful faces in a hemianopic patient (with unilateral destruction of primary visual cortex) when he was exposed to emotional stimuli in his blind visual hemifield (de Gelder, Vroomen, Pourtois & Weiskrantz, 1999; Rossion, de Gelder, Pourtois, Guerit & Weiskrantz, 2000). This has led to the hypothesis that a neural route, by-passing the striate cortex, might reach the amygdala using a subcortical visual pathway from the lateral geniculate nucleus (LGN) through the pulvinar and superior colliculus. Enroth-Cugell & Robson (1966) reported the spatiotemporal characteristics of X (responding to high- resolution stimuli) and of Y (responding to low-resolution stimuli) retinal ganglion cells; they showed that, following retinal processing, there is a difference between high and low spatial frequencies. Hubel & Wiesel (1977) reported that this distinction remains for the lateral geniculate nucleus: the magnocellular layers receiving preferentially projections from Y retinal ganglion cells, whereas X cells project to both parvo and magnocellular layers. Formally, in the visual thalamus, the magnocellular layer is equivalent to a high-pass filter in the temporal frequency domain and a low-pass filter in the spatial frequency domain. Thus, magnocellular neurons mainly provide rapid but low spatial frequency (LSF) information encoding configural features, as well as brightness and motion of objects; whereas the parvocellular neurons provide slower but high spatial frequency (HSF) information about local shape features, color, and texture. Testing the role of magnocellular inputs in fearful face recognition, Vuilleumier, Armony, Driver & Dolan (2003) conducted a functional magnetic resonance imaging (fMRI) experiment in which human observers were exposed to different spatial frequency components of faces (i.e. LSF only, HSF only, or the integral broad spatial frequency (BSF) images), with either a fearful or a neutral expression. Results showed that HSF and BSF faces produced more activation of the fusiform cortex than LSF faces, irrespective of expression; this suggests predominant contribution of the parvocellular information to the ventral visual stream for face identification. In contrast, the amygdala and subcortical tecto-pulvinar areas were “blind” to the difference of expressions conveyed by HSF information, but selectively activated by fearful relative to neutral faces seen in LSF or BSF images; this suggests an important role of magnocellular information for the activation of amygdala-related circuits in face emotion recognition. The purpose of the present paper is to examine the usefulness of LSF cues in fearful face recognition by comparing the performance of a distributed neuronal and a statistical models of visual processing exposed to different spatial frequency information. We tested how facial information provided by LSF and HSF images influenced two different computational models for an emotional classification task of face images.