The results of this study demonstrate that individuals with high levels of anxious apprehension tend to have slower transfer of angry face information from the left to the right hemisphere, compared to individuals with lower levels of anxious apprehension. The groups did not differ in interhemispheric transfer of happy or neutral faces. Further, state anxiety was uncorrelated with interhemispheric transfer times, indicating that the effect was specific to worry-related aspects of anxiety. These results support the idea that altered interhemispheric communication of threatening information may be one neural mechanism of cognitive avoidance in individuals prone to worry.
These results conceptually replicate and extend earlier findings of altered interhemispheric communication in worriers. An earlier study (Compton et al., 2004
) used a behavioral paradigm that required participants to match pictures of facial expressions either within or between the hemispheres. Worriers tended to match angry faces less accurately in a condition in which the left hemisphere had to transfer the angry face information to the right hemisphere. Although behavioral performance in bilateral matching paradigms is correlated with interhemispheric transfer times (especially from the left to right hemisphere; Larson & Brown, 1997
), the behavioral method is limited in its ability to assess interhemispheric dynamics. Interhemispheric communication is not measured directly in the behavioral paradigm, but rather inferred from patterns of within-and between-hemisphere matching performance. To address this limitation, the present study used an ERP method of measuring interhemispheric transfer time. Across the whole sample, peak N170 latencies occurred earlier over the contralateral than the ipsilateral hemisphere, replicating earlier data (e.g., Rugg et al., 1984
; Saron & Davidson, 1989
). Because ipsilateral peaks are typically absent in those with callosal sections or callosal agenesis (Bayard, Gosselin, Robert, & Lassonde, 2004
; Brown, Jeeves, Dietrich, & Burnison, 1999
; Rugg, Milner, & Lines, 1985
), we can assume that ipsilateral peaks depend upon an intact callosum, and that time lags between contralateral and ipsilateral peaks reflect callosal transfer. Therefore, the individual differences reported in this study likely reflect individual differences in the timing of information transfer across the callosum.
These results suggest one possible neural mechanism for cognitive avoidance in people who are prone to worry. The cognitive avoidance hypothesis was originally developed based on the self-reported characteristics of worriers, and has received further support from studies showing that worry reduces autonomic responses to threats (Borkovec et al., 1998
). Studies demonstrating enhanced left frontal activity in those with high anxious apprehension (Carter et al., 1986
; Engels et al., 2007
; Heller et al., 1997
; Hofmann et al., 2005
) are consistent with the verbal nature of cognitive avoidance in anxious apprehension. The present results complement and extend these prior findings by demonstrating that it is not just regional brain activity levels, but also communication of information between brain regions that differs between worriers and non-worriers. Reduced left-to-right communication of threatening images in worriers may provide a link that connects increased left-hemisphere activity with reduced autonomic responses, which are presumably controlled by the right hemisphere (e.g., Dalton et al., 2005
; Wittling, 1995
While prior studies of the neural basis of anxious apprehension have focused on asymmetries in frontal lobe regions, the present results involve interhemispheric exchange between posterior regions that are involved in perceptual processing. These two lines of research should be seen as complementary. It is plausible that a verbally-dominated strategy of avoidance could involve both increased left frontal activity (Engels et al., 2007
) and an altered pattern of interhemispheric communication between posterior regions. Frontal lobe regions are known to exert top-down control over subcortical and cortical regions, including temporal cortex regions that represent visual images such as faces (e.g., Gazzaley, Cooney, McEvoy, Knight, & D’Esposito, 2005
; Gazzaley et al., 2007
). Such frontally-mediated control can establish a mental set that influences how information is processed in posterior regions (e.g., Miller & Cohen, 2001
). Therefore, a cognitive strategy of threat avoidance in worry-prone people may involve activation of left-frontal systems that alter processing in the temporal regions that process visual image information.
Altered interhemispheric exchange is unlikely to be the only neural mechanism contributing to avoidance in anxiety. The transfer time effects were small in magnitude, implying that other mechanisms probably play a role in cognitive avoidance as well. For example, one study found that during an induced worry condition, cerebral blood flow increased in a left frontal lobe region and decreased in limbic structures such as the amygdala (Hoehn-Saric, Lee, McLeod, & Wong, 2005
). These neuroimaging results suggest that worry may involve top-down regulation of subcortical regions by frontal regions, a possibility that is not mutually exclusive with the interhemispheric mechanism that we propose.
In addition to implications regarding cognitive avoidance in anxiety, the present results also underscore the importance of conceptualizing interhemispheric communication as a dynamic process, rather than a fixed information relay. Behavioral studies of interhemispheric interaction have long emphasized its dynamic nature. For example, researchers have conceived of the callosum as a selective filter that can adaptively control information flow between the hemispheres (e.g., Liederman, 1986
; Mikels & Reuter-Lorenz, 2004
; Weissman & Banich, 1999
). Studies using behavioral methods have shown that interhemispheric communication is modulated by changing task demands (Weissman & Banich, 2000
) and situational factors such as evaluation stress (Compton & Mintzer, 2001
; Compton et al., 2004
). In contrast, most ERP studies have tended to view interhemispheric transfer time as relatively fixed within a person, and individual differences in transfer time have often been viewed as reflecting anatomical differences between people (e.g., Barnett, Corballis, & Kirk, 2005
; Moes, Brown, & Minnema, 2007
; Patston, Kirk, Rolfe, Corballis, & Tippett, 2007
; though see Nowicka, Grabowska, & Fersten, 1996
). The present results suggest that individual differences in transfer time can be dependent on stimulus type, because the significant anxiety-related results were limited to angry faces. These data fit with a conception of interhemispheric communication as an active, selective process rather than a passive relay based on fixed anatomy.
While the pattern of contralateral versus ipsilateral latencies in the whole sample was robustly significant in the anatomically-predicted direction, a fraction of participants had anatomically impossible transfer times, and these participants had to be excluded in order for anxiety-related effects to be evident. This is one limitation of the current dataset. However, the percentage of participants with anatomically-impossible transfer times in our study was comparable to percentages reported in earlier research (Saron & Davidson, 1989
). This most likely points to a general limitation of the ERP method of studying interhemispheric transfer, rather than a problem with how we implemented that method. Anatomically-incorrect transfer times may arise from a variety of sources, such as a waveform with a poorly defined peak, latency jitter, an atypically oriented dipole, or slight asymmetries in the correspondence between the electrode site on the scalp and the underlying cortex. It is possible that with larger samples of high and low worriers, participants with erroneous transfer times could still be included and have less statistical impact on the overall group comparison. However, in the present study, individual differences in anxiety were only evident when those with erroneous transfer times were excluded.
Another limitation of the ERP method is that it focuses on interhemispheric communication within a certain time frame, that is the initial volleys of sensory-perceptual information exchange measured within the first 200 ms following stimulus presentation. Sharing of perceptual information is necessary to construct a unified perception of both sides of visual space and likely takes place over posterior sections of the callosum (Brown et al., 1999
). However, information exchange across the callosum is not limited to this stage of processing or this anatomical sector, but rather involves many channels and many temporal stages (for reviews, see Banich, 2003
; Clarke, 2003
; Innocenti & Bressoud, 2003
; Saron, Foxe, Simpson, & Vaughan, 2003
). While the present study has demonstrated associations between anxiety and one aspect of callosal transfer, other aspects of callosal exchange are less amenable to measurement with the ERP transfer time method, and should be addressed with other methods in the future. In addition, the present method examines the brain’s initial response to externally presented stimuli, whereas worry is likely to influence the internal generation of threat-related imagery as well (e.g., Behar et al., 2005
). Although perception and imagery are generally thought to rely upon similar neural systems (e.g., Behrmann, 2000
; Ganis, Thompson, Mast, & Kosslyn, 2004
), the relation between perceptual processing and imagery in the context of anxiety worry deserves future research attention.
Future studies can extend these results in a number of potentially fruitful directions. First, it would be beneficial to tie interhemispheric dynamics more directly to tonic levels of activity measured with EEG or hemodynamic measures. For example, worriers with higher levels of left frontal activity may also show more altered interhemispheric exchange, if the same verbalization strategy drives both the activity level and the interhemispheric dynamics. Researchers could also test whether autonomic responses to threatening images are lessened in those who display reduced left-to-right hemisphere exchange, tying interhemispheric processing even more directly to ongoing research on cognitive avoidance (Borkovec et al., 2004
). In addition, a worry-induction paradigm could be used to determine whether individual differences in interhemispheric effects are due to trait differences, activation of a worry strategy, or some combination. In the present study, interhemispheric transfer effects were uncorrelated with state anxiety, suggesting a crucial role for trait differences in anxious apprehension. At the same time, the effect may be enhanced among worriers when they actively engage in worry, compared to baseline conditions. A study that manipulated state levels of worry could more directly address this issue.
Finally, while the present study focused on individual differences among a nonclinical undergraduate sample, future studies could examine individuals with generalized anxiety disorder (GAD). GAD is characterized by high levels of worry symptoms (Borkovec et al., 2004
), along with the additional tendency towards “meta-worries”, or worries about worrying (Wells, 2004
). Future research could help to determine whether GAD samples are qualitatively different than non-pathological high worriers or whether the two share common neural mechanisms of threat avoidance.
In sum, the present results add to our understanding of the neural basis of anxiety by demonstrating that information exchange between the hemispheres, particularly for threatening information, is altered in individuals with the propensity to worry. These results fit with an influential theory of cognitive avoidance in anxiety derived from the clinical literature (Borkovec et al., 2004
). In addition, the results support a view of the corpus callosum as a selective filter that shapes information processing in ways that are influenced by emotional variables such as trait individual differences and stimulus content. Future research can examine the relationship between interhemispheric exchange and other physiological correlates of anxious apprehension to test further the possibility that altered interhemispheric communication may contribute to avoidance strategies in anxious individuals.