Functional Evidence for a Dual Route to Amygdala

Marta I. Garrido, Gareth R. Barnes, Maneesh Sahani, Raymond J. Dolan
2012 Current Biology  
The amygdala plays a central role in evaluating the behavioral importance of sensory information. Anatomical subcortical pathways provide direct input to the amygdala from early sensory systems and may support an adaptively valuable rapid appraisal of salient information [1] [2] [3] . However, the functional significance of these subcortical inputs remains controversial [4] . We recorded magnetoencephalographic activity evoked by tones in the context of emotionally valent faces and tested two
more » ... mpeting biologically motivated dynamic causal models [5, 6] against these data: the dual and cortical models. The dual model comprised two parallel (cortical and subcortical) routes to the amygdala, whereas the cortical model excluded the subcortical path. We found that neuronal responses elicited by salient information were better explained when a subcortical pathway was included. In keeping with its putative functional role of rapid stimulus appraisal, the subcortical pathway was most important early in stimulus processing. However, as often assumed, its action was not limited to the context of fear, pointing to a more widespread information processing role. Thus, our data supports the idea that an expedited evaluation of sensory input is best explained by an architecture that involves a subcortical path to the amygdala. Results Our goal was to assess the explanatory power of a fast subcortical route in salient information processing. We first investigated whether brain responses elicited by a salient context, such as unpredictable information under threat, were better modeled with or without a subcortical "low route." We hypothesized that early evoked responses would be better explained by the dual-route model and predicted that a subcortical pathway would play a more significant role in early, rather than later, time epochs. The critical factor in such a model is rapidity of processing, and this mandates a methodology with adequate temporal resolution. Thus, we used computational modeling to compare models, with and without the subcortical pathway, and evaluated their predictions in terms of how well they explained evoked magnetoencephalographic (MEG) data. In addition, we asked whether the functional role of the subcortical pathway depends on stimulus predictability and emotional context. This provides an opportunity to address an unresolved and controversial question as to the degree to which subcortical processing promotes expeditious evaluation of biological significance in sensory information. Surprise-Evoked Fields Are Enhanced in a Fearful Context We presented participants with a sequence of predictable and surprising pure tone sounds. Subjects simultaneously performed a gender discrimination task on visually presented faces with neutral, happy, or fearful expressions (Figure 1 ). Responses to predictable, or standard, sounds were similar in all three contexts. However, the strength of the fields evoked by oddballs, or surprising events, increased with the emotional salience of facial expressions. This gradient was particularly evident in the period of 100-150 ms poststimulus, with the largest effect being evident in the context of fearful faces, consistent with previous studies [7] (Figure 2A ). Enhanced Early Amygdala Activity with a Subcortical Pathway We estimated that activity at each source included in two competing dynamic causal models (DCMs) [5] for oddballs under fear ( Figure 2C and 2D ). The cortical model (C) included a cortical pathway only, which tests a hypothesis that information about auditory objects reaches the amygdala after being processed by the auditory thalamus (MGB) and primary auditory cortex (A1). On the other hand, a dual-route, or cortical and subcortical model (CS), included a cortical and subcortical pathway, expressing a hypothesis that information reaches the amygdala both directly through a thalamic projection and indirectly through a cortical route ( Figure 2D ). Activity in A1 as estimated by both models was similar. Crucially, we found that the dual-route model could recover early amygdala activity (peaking at w50 ms and w100 ms). Conversely, the absence of the subcortical pathway linking MGB to AMY caused early (<100 ms) amygdala activity to disappear. The cortical model could only recover late amygdala activity (peaking at about 150 ms) ( Figure 2C ). This dissociation supports the role of a subcortical pathway in conveying rapid information to the amygdala. Time-Specific Role of the Subcortical Pathway Neuroanatomical tracings in the rat demonstrate the existence of two parallel processing pathways involving a thalamocortico-amygdala and a direct thalamo-amygdala pathway [8] . There is also evidence that auditory inputs can access the basolateral amygdala from both the auditory thalamus and the cortex [9] [10] [11] . Crucially, direct subcortical connections between the auditory thalamus and the amygdala are alone sufficient for some forms of fear conditioning [12] [13] [14] . On this basis it is argued that a subcortical pathway plays an important role in adaptive behavior. Indeed, the ability to rapidly process behaviorally relevant information represents a biological advantage in a potentially dangerous environment. Hence, a fast route that bypasses cortical processing is central to the dual-route hypothesis [2] . Motivated by this and the source analysis described above ( Figure 2C ), we asked whether the relevance of the subcortical pathway was dependent on time. We hypothesized that the functional role of the subcortical pathway is crucial at early processing stages and
doi:10.1016/j.cub.2011.11.056 pmid:22209532 pmcid:PMC3267035 fatcat:bm7whkf6inc7dda5ewiy3cwgpq