Bilateral dorsal and ventral fiber pathways for the processing of affective
prosody identified by probabilistic fiber tracking
Sascha Frühholz
a,b,
⁎, Markus Gschwind
c,d
, Didier Grandjean
a,b
a
Neuroscience of Emotion and Affective Dynamics Laboratory, Department of Psychology, University of Geneva, Geneva, Switzerland
b
Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland
c
Laboratory of Neurology and Imaging of Cognition, Department of Neurosciences, University of Geneva, Geneva, Switzerland
d
Neurology Service, Department of Clinical Neurosciences, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
abstract article info
Article history:
Accepted 2 January 2015
Available online 9 January 2015
Keywords:
Emotion
Prosody
Voice
DTI
Probabilistic fiber tracking
Auditory pathways
Dorsal and ventral pathways for syntacto-semantic speech processing in the left hemisphere are represented in
the dual-stream model of auditory processing. Here we report new findings for the right dorsal and ventral
temporo-frontal pathway during processing of affectively intonated speech (i.e. affective prosody) in humans, to-
gether with several left hemispheric structural connections, partly resembling those for syntacto-semantic
speech processing. We investigated white matter fiber connectivity between regions responding to affective
prosody in several subregions of the bilateral superior temporal cortex (secondary and higher-level auditory cor-
tex) and of the inferior frontal cortex (anterior and posterior inferior frontal gyrus). The fiber connectivity was
investigated by using probabilistic diffusion tensor based tractography. The results underscore several so far
underestimated auditory pathway connections, especially for the processing of affective prosody, such as a
right ventral auditory pathway. The results also suggest the existence of a dual-stream processing in the right
hemisphere, and a general predominance of the dorsal pathways in both hemispheres underlying the neural pro-
cessing of affective prosody in an extended temporo-frontal network.
© 2015 Elsevier Inc. All rights reserved.
Introduction
Cortical auditory processing involves several perisylvian regions,
which are interconnected by different fiber pathways. Recent studies
(Friederici et al., 2006; Rauschecker and Scott, 2009; Saur et al., 2008)
have predominantly identified left hemispheric processing pathways
within a dual-stream model of auditory processing (Hickok and
Poeppel, 2007). They include ventral pathways from anterior superior
temporal gyrus (STG) to the anterior inferior frontal gyrus (IFG) and
dorsal pathways, which project to the posterior IFG via the posterior
STG (Hickok and Poeppel, 2007; Rauschecker and Scott, 2009). Especial-
ly the dorsal pathway seems strongly left lateralized (Hickok and
Poeppel, 2007). The ventral pathways convey sound-invariant meaning
(Belin and Zatorre, 2000b; Rauschecker and Scott, 2009), such as speech
semantics (Hagoort, 2005). The dorsal pathways serve sound-to-motor
mapping (Saur et al., 2008) and the processing of temporal auditory se-
quences (Belin and Zatorre, 2000b; Rauschecker and Scott, 2009),
which are also necessary for the understanding of speech syntax
(Friederici et al., 2006). Compared to a predominant role of the left
brain for syntacto-semantic processing (Specht, 2014), the emotional
intonation in speech, that is the affective prosody, strongly, but not ex-
clusively, activates regions in right STG and IFG (e.g. Alba-Ferrara et al.,
2011; Beaucousin et al., 2007; Ethofer et al., 2006; Fruhholz et al., 2012).
Thus, investigating the neural basis of affective prosody processing pro-
vides an ideal paradigm to investigate right hemispheric auditory path-
ways using diffusion-weighted imaging techniques together with
functional magnetic resonance imaging.
These temporo-frontal pathways for affective prosody processing
have been rarely studied (Ethofer et al., 2012; Glasser and Rilling,
2008), mainly pointing to a right dorsal pathway (Gharabaghi et al.,
2009; Glasser and Rilling, 2008), but also providing evidence for the
possibility of a right ventral pathway (Ethofer et al., 2012). However,
these studies explored pathways, first, only for circumscribed temporal
regions, second, without specifying frontal target regions, third, without
quantifying the architecture of these pathways, and therefore without
dissociating the different possible functional roles of these pathways
(Ethofer et al., 2012; Glasser and Rilling, 2008). Taken together, these
critical points might have led to a considerable underestimation of the
importance and complexity of the temporo-frontal white matter path-
way connectivity. Ventral and dorsal pathways, for example, are sup-
posed to originate in multiple STG seed regions (Friederici, 2011;
Fruhholz et al., 2012). Furthermore, these pathways probably terminate
in the anterior as well as in the posterior IFG (Fruhholz and Grandjean,
2013b), serving to evaluate (Schirmer and Kotz, 2006) and to categorize
NeuroImage 109 (2015) 27–34
⁎ Corresponding author at: Swiss Center for Affective Sciences University of Geneva, 9
Chemin des Mines, CH-1202 Geneva, Switzerland.
E-mail address: sascha.fruehholz@unige.ch (S. Frühholz).
http://dx.doi.org/10.1016/j.neuroimage.2015.01.016
1053-8119/© 2015 Elsevier Inc. All rights reserved.
Contents lists available at ScienceDirect
NeuroImage
journal homepage: www.elsevier.com/locate/ynimg