Functional Dissociation between Medial and Lateral Prefrontal Cortical Spatiotemporal Activation in Negative and Positive Emotions: A Combined fMRI/MEG Study

Abstract

The orbitofrontal cortex has been cytoarchitectonically and connectionally subdivided into a medial and a lateral part which are assumed to subserve distinct functions in emotional processing. However the exact spatiotemporal mechanisms of negative and positive emotional processing in medial and lateral orbitofrontal cortex remain unclear. We therefore investigated spatiotemporal orbitofrontal and prefrontal cortical activation patterns during emotional stimulation in a combined fMRI/MEG study. We investigated 10 healthy subjects, 5 women and 5 men. Positive and negative pictures from the International Affective Picture system (IAPS) were used for emotional stimulation, whereas neutral and gray pictures were taken as control conditions. fMRI/MEG measurements covered the whole frontal lobe and a time window between -2000 and +200 ms around motor responses (right index finger extension) associated with each picture. Positively and negatively correlated activities were determined in various prefrontal/frontal cortical regions in fMRI. Isocontour maps and single dipoles in MEG were analyzed in 50 ms time windows ranging from -2000 to +200 ms. Dipoles and fMR images were mapped on three-dimensional anatomical MRI so that anatomical localization of single dipoles and regional fMRI activity could be compared. Both negative and positive emotional conditions differed from non-emotional control conditions by strong orbitofrontal and lateral prefrontal activation as well as by the presence of early magnetic fields (-1700 to +1100 ms). Negative emotional processing was characterized by strong medial orbitofrontal activation and earlier (-1700 ms), stronger and more medially oriented orbitofrontal dipoles. In contrast positive emotional processing showed a rather strong activation in lateral prefrontal cortex with later (-1500 ms), weaker and more laterally oriented orbito and prefrontal dipoles. Negative emotional processing can be characterized by strong and early medial orbitofrontal cortical activation, whereas positive emotional processing showed rather later and weaker activation in lateral orbitofrontal/prefrontal cortex. Such a functional dissociation between medial and lateral orbito-frontal/prefrontal cortex during negative and positive emotional processing lends further support to the assumption of a functional subdivision in the orbitofrontal cortex.

Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder

“…Single-unit recording in human orbital frontal cortex showed increased firing rates to aversive stimuli including facial expressions of fear (32). Similar increases in orbital frontal activity were measured with functional imaging to angry expressions (33), to aversive stimuli (34), and to the actual induction of anger (35,36). Disruption of the medial prefrontal cortex by transcranial magnetic stimulation caused a delay in the recognition of angry faces but not happy faces (37).…”

Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle

“…This finding has supported a model whereby the medial orbitofrontal cortex codes for pleasantness and the lateral orbitofrontal cortex codes for unpleasantness (16). However, running counter to this model, some studies have found increased medial OFC activity to negative stimuli or increased lateral OFC activity to positive stimuli (17)(18)(19). These conflicting results indicate that, for valance encoding in the OFC, the distinction between medial and lateral might be not as simple as the encoding of positive as opposed to negative stimuli and might depend on stimulus modality and complex aspects of stimulus processing.…”

“…However, some studies have found medial OFC activity to negative stimuli or lateral OFC activity to positive stimuli (17)(18)(19). Key issues in understanding these discrepancies include sensory modalities of presented stimuli, stimulus characteristics that may confound valence differences, and individual subject differences, such as menstrual cycle phase in female subjects.…”

Frontal lobe hypoactivation in medication-free adults with bipolar II depression during response inhibition

“…These regions share extensive reciprocal connections with the amygdala, anterior temporal and anterior cingulate cortex (Ongur and Price, 2000). Functional neuroimaging studies in healthy subjects have demonstrated a role for the medial and lateral sectors of the IFC in mood regulation (Baker et al, 1997;Northoff et al, 2000) and in emotional memory (Cabeza and Nyberg, 2000). It has been speculated that the IFC is involved in the highest level of behavior regulation, including emotion regulation, through pathways between the IFC and autonomic systems that govern visceral responses associated with affective stimuli (Cabeza and Nyberg, 2000).…”