Neuropsychologia 45 (2007) 1187–1195
An electrophysiological study on the interaction between emotional
content and spatial frequency of visual stimuli
Luis Carreti´ e
a,∗
, Jos´ e A. Hinojosa
b
, Sara L ´ opez-Mart´ ın
a
, Manuel Tapia
a
a
Facultad de Psicolog´ ıa, Universidad Aut´ onoma de Madrid, 28049 Madrid, Spain
b
Instituto Pluridisciplinar, Universidad Complutense de Madrid, 28040 Madrid, Spain
Received 9 March 2006; received in revised form 11 September 2006; accepted 24 October 2006
Available online 22 November 2006
Abstract
Previous studies suggest that the magnocellular pathway, a visual processing system that rapidly provides low spatial frequency information to
fast-responding structures such as the amygdala, is more involved in the processing of emotional facial expressions than the parvocellular pathway
(which conveys all spatial frequencies). The present experiment explored the spatio-temporal characteristics of the spatial frequency modulation
of affect-related neural processing, as well as its generalizability to non-facial stimuli. To that aim, the event-related potentials (ERPs) elicited by
low-pass filtered (i.e., high spatial frequencies are eliminated) and intact non-facial emotional images were recorded from 31 participants using a
60-electrode array. The earliest significant effect of spatial frequency was observed at 135 ms from stimulus onset: N135 component of the ERPs.
In line with previous studies, the origin of N135 was localized at secondary visual areas for low-pass filtered stimuli and at primary areas for intact
stimuli. Importantly, this component showed an interaction between spatial frequency and emotional content: within low-pass filtered pictures,
negative stimuli elicited the highest N135 amplitudes. By contrast, within intact stimuli, neutral pictures were those eliciting the highest amplitudes.
These results suggest that high spatial frequencies are not essential for the initial affect-related processing of visual stimuli, which would mainly
rely on low spatial frequency visual information. According to present data, high spatial frequencies would come into play later on.
© 2006 Elsevier Ltd. All rights reserved.
Keywords: ERPs; Visual cortex; Principal component analysis; Aversive stimulation; Magnocellular; Parvocellular
1. Introduction
Survival requires organisms to process the environment accu-
rately and reliably, but also to react rapidly, at the cost of
some precision, to certain biologically important events. This
dual capability is favoured by the existence of two different
neural systems for processing visual information. The mag-
nocellular pathway carries low-quality visual information but
rapidly distributes it to fast-responding areas such as the pre-
frontal cortex (Bar, 2003; Bar et al., 2006) or the amygdala
(Vuilleumier, Armony, Driver, & Dolan, 2003), thus allowing
an urgent response that may be critical for coping with biologi-
cally significant stimulation. On the other hand, the parvocellular
pathway, while being precise, is exclusively directed towards
visual cortex (Merigan & Maunsell, 1993), allowing a deep
exploration of the stimulation. A key visual feature that distin-
∗
Corresponding author. Fax: +34 91 4975215.
E-mail address: carretie@uam.es (L. Carreti´ e).
guishes the ‘style of processing’ of these two visual systems is
spatial frequency. The magnocellular pathway conveys mainly
low frequencies, which provide only gross information about
the shape of an object, while the parvocellular pathway carries
all spatial frequencies, necessary for the processing of details
such as edges, or small visual elements or contrasts.
Rapid motor and autonomic responses to emotional events
are organized by the amygdala (e.g., LeDoux, 2000). Several
data indicate that high spatial frequencies are not essential for
the amygdala to be activated, suggesting that this structure is
able to process, at least in some phases, magnocellular informa-
tion exclusively: low-pass filtered emotional facial expressions
(i.e., faces which only present low spatial frequencies) elicit a
greater activation of this structure than emotional expressions
containing high frequencies (Vuilleumier et al., 2003). This is
an adaptive neural strategy, since emotional stimuli often require
urgent responses. Convergently, haemodynamic studies consis-
tently show that the activity of the human amygdala increases
to a higher extent in response to emotional stimuli, particularly
negative, than in response to non-emotional stimuli (see reviews
0028-3932/$ – see front matter © 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2006.10.013