Elsevier

Neuroscience

Volume 277, 26 September 2014, Pages 229-238
Neuroscience

The timing and directional connectivity of human frontoparietal and ventral visual attention networks in emotional scene perception

https://doi.org/10.1016/j.neuroscience.2014.07.005Get rights and content

Highlights

  • Rapid neuroimaging used to assess the timing of human emotional scene perception.

  • Amygdala and fusiform gyrus show comparatively early emotional discrimination.

  • Frontoparietal network shows comparatively late emotional discrimination.

  • Causal connectivity analyses indicate that the amygdala directs the fusiform gyrus.

Abstract

Electrocortical and hemodynamic measures reliably identify enhanced activity in the ventral and dorsal visual cortices during the perception of emotionally arousing versus neutral images, an effect that may reflect directive feedback from the subcortical amygdala. However, other brain regions strongly modulate visual attention, such as frontal eye fields (FEF) and intraparietal sulcus (IPS). Here we employ rapid sampling of BOLD signal (4 Hz) in the amygdala, fusiform gyrus (FG), FEF and IPS in 42 human participants as they viewed a series of emotional and neutral natural scene photographs balanced for luminosity and complexity, to test whether emotional discrimination is evident in dorsal structures prior to such discrimination in the amygdala and FG. Granger causality analyses were used to assess directional connectivity within dorsal and ventral networks. Results demonstrate emotionally-enhanced peak BOLD signal in the amygdala, FG, FEF, and IPS, with the onset of BOLD signal discrimination occurring between 2 and 3 s after stimulus onset in ventral structures, and between 4 and 5 s in FEF and IPS. Granger causality estimates yield stronger directional connectivity from IPS to FEF than the reverse in this emotional picture paradigm. Consistent with a reentrant perspective of emotional scene perception, greater directional connectivity was found from the amygdala to FG compared to the reverse. These data support a perspective in which the registration of emotional scene content is orchestrated by the amygdala and rostral inferotemporal visual cortex.

Introduction

Electrocortical and hemodynamic measures reveal enhanced activity in ventral and dorsal visual cortices during emotional relative to neutral picture perception (Pourtois et al., 2004, Sabatinelli et al., 2005, Pessoa et al., 2006, Anticevic et al., 2011, Sabatinelli et al., 2013, Wiens and Syrjanen, 2013), an effect that may reflect a natural selective attention to behaviorally relevant stimuli (Vuilleumier and Driver, 2007, Lang and Bradley, 2010, Pessoa and Adolphs, 2010, Markovic et al., 2013). Some evidence suggests an association between enhanced fusiform gyrus (FG) activity and directive feedback from the subcortical amygdala (Armony and Dolan, 2002, Vuilleumier et al., 2004, Sabatinelli et al., 2005, Sabatinelli et al., 2009).

However, other brain regions strongly modulate visual attention, such as frontal eye fields (FEF) and intraparietal sulcus (IPS) (Rizzolatti et al., 1987, Corbetta, 1998, Schafer and Moore, 2007, Bisley and Goldberg, 2010). This frontoparietal (FP) network is persistently involved in a process of categorizing stimulus relevance and directing the locus of visual attention (Corbetta et al., 2008). While the characteristics of this FP network have been thoroughly investigated in target-driven visuospatial attention tasks (Serences and Yantis, 2006) the role of stimulus emotion on the engagement of this network is underexplored. While studies have demonstrated that emotional stimuli evoke augmented FP activity (Moratti et al., 2004, Sabatinelli et al., 2007a, Sabatinelli et al., 2007b, Shafer and Dolcos, 2012, Brosch and Grandjean, 2013, Ferri et al., 2013), the mechanisms by which emotional characteristics modulate FP activity are poorly defined (Adolphs, 2002, Mitchell et al., 2008, Vuilleumier and Huang, 2009, Frank and Sabatinelli, 2012).

One means of addressing research questions regarding the temporal order of human brain activity is through comparisons of the relative timing of the BOLD signal within a structure across experimental conditions. While the BOLD signal is inherently delayed and smoothed relative to neural activity, the timing of signal change within active clusters is highly reliable (Kim et al., 1997, Menon and Kim, 1999, Miezin et al., 2000, Lin et al., 2013). Here we sample the BOLD contrast four times per second in 4-slice slabs of ventral (amygdala and FG) and dorsal (FEF and IPS) brain regions during an emotional and neutral picture series to test whether emotional discrimination is apparent in the FP network prior to such emotional discrimination in the amygdala and FG. There is evidence for a rapid response latency in human (Kirchner et al., 2009) and macaque (Schmolesky et al., 1998) FEF, and human data that suggest a role for FEF in modulating attention enhancement in the visual cortex (Taylor et al., 2007). If picture stimulus emotion is discriminated in the FP network prior to the amygdala and FG, a reentrant perspective of emotional perception (Freese and Amaral, 2005, Sabatinelli et al., 2009, Vuilleumier and Huang, 2009) would not be supported. If emotional discrimination is apparent in the amygdala and FG prior to such discrimination in the FP network, the emotionally-enhanced activity seen in FP structures during scene perception may reflect input from the amygdala and FG, or other regions not yet sampled.

Rapid sampling also provides an opportunity to determine potential asymmetries in directional connectivity between structures within the ventral and dorsal networks using Granger connectivity analyses. As there is support for a directive effect of the amygdala on FG (Anderson and Phelps, 2001, Vuilleumier and Driver, 2007, Sabatinelli et al., 2009) and for the FEF on IPS (Bressler et al., 2008), the current data will enable a test of these hypothesized directional connectivities in an emotional picture perception task.

Section snippets

Participants and procedure

Forty-five undergraduate students from the University of Georgia participated in the experiment, receiving $20 USD compensation. Three subjects’ data were lost due to MR scanner or stimulus presentation equipment malfunction. Of the 42 participants (average age 22 years, standard deviation (SD) 3) in the final sample, 20 were female. All participants gave informed consent, and this study was approved by the University of Georgia Human Subjects Review Board. All participants reported no

Stimulus ratings

Averages and standard errors of valence and arousal ratings for the 80 picture stimuli used in this study are shown in Table 1. The ratings for the 20 picture stimuli selected from the International Affective Picture System (IAPS) are drawn from the normative values (also drawn from undergraduate sample) published in the IAPS technical manual (Lang et al., 2008), and differed reliably across valence (F (2, 17) = 69.00, p < .001) with pleasant stimuli yielding higher valence ratings relative to

Discussion

Assessing the relative contributions of dorsal and ventral structures to the process of emotional discrimination in humans is methodologically challenging, as high levels of spatial and temporal resolution are necessary, and direct access to all structures of interest via invasive methods is extremely rare. Moreover, ventromedial cortical and subcortical regions present a particularly weak signature in the noninvasive electro- and magneto-encephalogram. One means of addressing the research

Study limitations

Our primary goal in this experiment was to determine if the emotional discrimination we knew to exist in the FP network preceded such discrimination in the amygdala and FG. While it may be tempting to interpret the relative timing of emotional discrimination as suggesting a hierarchy from ventral to dorsal structures, the current data cannot speak of this relationship directly, as these regions were sampled at different times. Moreover, GC analyses were performed to address separate questions

Conflict of interest

The authors declare no competing financial interests.

References (85)

  • K.A. Dyckman et al.

    An effect of context on saccade-related behavior and brain activity

    Neuroimage

    (2007)
  • D.A. Feinberg et al.

    Ultra-fast MRI of the human brain with simultaneous multi-slice imaging

    J Magn Res

    (2013)
  • K.J. Friston et al.

    Event-related fMRI: characterizing differential responses

    Neuroimage

    (1998)
  • C.R. Genovese et al.

    Thresholding of statistical maps in functional neuroimaging using the false discovery rate

    Neuroimage

    (2002)
  • S.G. Kim et al.

    Limitations of temporal resolution in functional MRI

    Magn Reson Med

    (1997)
  • V.A. Lamme et al.

    The distinct modes of vision offered by feedforward and recurrent processing

    Trends Neurosci

    (2000)
  • P.J. Lang et al.

    Emotion and the motivational brain

    Biol Psychol

    (2010)
  • F.-H. Lin et al.

    fMRI hemodynamics accurately reflects neuronal timing in the human brain measured by MEG

    Neuroimage

    (2013)
  • E. Maris et al.

    Nonparametric statistical testing of EEG-and MEG-data

    J Neurosci Methods

    (2007)
  • R.S. Menon et al.

    Spatial and temporal limits in cognitive neuroimaging with fMRI

    Trends Cogn Sci

    (1999)
  • F.M. Miezin et al.

    Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing

    Neuroimage

    (2000)
  • D.G. Mitchell et al.

    The interference of operant task performance by emotional distracters: an antagonistic relationship between the amygdala and frontoparietal cortices

    Neuroimage

    (2008)
  • H. Nishijo et al.

    Neural correlates to both emotion and cognitive functions in the monkey amygdala

    Behav Brain Res

    (2008)
  • T. Paus

    Location and function of the human frontal eye-field: a selective review

    Neuropsychologia

    (1996)
  • G. Rizzolatti et al.

    Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention

    Neuropsychologia

    (1987)
  • D. Sabatinelli et al.

    Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance

    Neuroimage

    (2005)
  • D. Sabatinelli et al.

    Emotional perception: meta-analyses of face and natural scene processing

    Neuroimage

    (2011)
  • D. Sabatinelli et al.

    Emotional perception: correspondence of early and late event-related potentials with cortical and subcortical functional MRI

    Biol Psychol

    (2013)
  • R.J. Schafer et al.

    Attention governs action in the primate frontal eye field

    Neuron

    (2007)
  • J.T. Serences et al.

    Selective visual attention and perceptual coherence

    Trends Cogn Sci

    (2006)
  • S. Wiens et al.

    Directed attention reduces processing of emotional distracters irrespective of valence and arousal level

    Biol Psychol

    (2013)
  • A.K. Anderson et al.

    Lesions of the human amygdala impair enhanced perception of emotionally salient events

    Nature

    (2001)
  • K.M. Armstrong et al.

    Selection and maintenance of spatial information by frontal eye field neurons

    J Neurosci

    (2009)
  • C.L. Asplund et al.

    A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention

    Nat Neurosci

    (2010)
  • J.W. Bisley et al.

    Attention, intention, and priority in the parietal lobe

    Annu Rev Neurosci

    (2010)
  • S.L. Bressler et al.

    Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention

    J Neurosci

    (2008)
  • T. Brosch et al.

    Cross-modal modulation of spatial attention by emotion

  • R.B. Buxton et al.

    Dynamics of blood flow and oxygenation changes during brain activation: the balloon model

    Magn Reson Med

    (1998)
  • L. Carretie

    Exogenous (automatic) attention to emotional stimuli: a review

    Cogn Affect Behav Neurosci

    (2014)
  • M. Catani et al.

    Occipito-temporal connections in the human brain

    Brain

    (2003)
  • M. Corbetta

    Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems?

    Proc Natl Acad Sci USA

    (1998)
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nat Rev Neurosci

    (2002)
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