Subcortical Connections to Human Amygdala and Changes following Destruction of the Visual Cortex

Abstract

Nonconscious [1-6], rapid [7, 8], or coarse [9] visual processing of emotional stimuli induces functional activity in a subcortical pathway to the amygdala involving the superior colliculus and pulvinar. Despite evidence in lower mammals [10, 11] and nonhuman primates [12], it remains speculative whether anatomical connections between these structures exist in the human brain [13-15]. It is also unknown whether destruction of the visual cortex, which provides a major input to the amygdala, induces modifications in anatomical connections along this subcortical pathway. We used diffusion tensor imaging to investigate in vivo anatomical connections between human amygdala and subcortical visual structures in ten age-matched controls and in one patient with early unilateral destruction of the visual cortex. We found fiber connections between pulvinar and amygdala and also between superior colliculus and amygdala via the pulvinar in the controls as well as in the patient. Destruction of the visual cortex led to qualitative and quantitative modifications along the pathways connecting these three structures and the changes were confined to the patient's damaged hemisphere. The present findings thus show extensive neural plasticity in the anatomical connections between subcortical visual structures of old evolutionary origin involved in the processing of emotional stimuli.

From affective blindsight to emotional consciousness

“…Thus, it has been proposed, and later on verified with different neuroimaging methods, that considerable post-lesion and experience-dependent plasticity has taken place in GY's brain (Bridge et al, 2008;Tamietto et al, 2012). Although we will discuss the neural underpinnings of affective blindsight in a dedicated section below, it has become increasingly clear that affective blindsight is not such a rare phenomenon, for it has been reported in more than 20 different patients studied by at least five independent research teams in several different countries (Anders et al, 2004(Anders et al, , 2009Bertini et al, 2013;Cecere et al, 2014;de Gelder & Hadjikhani, 2006;de Gelder et al, 1999de Gelder et al, , 2002de Gelder et al, , 2005de Gelder et al, , 2014Hamm et al, 2003;Heywood & Kentridge, 2000;Morris et al, 2001;Pegna et al, 2005;Rossion et al, 2000;Tamietto & de Gelder, 2008;Tamietto et al, 2009Tamietto et al, , 2012Van den Stock et al, 2011). These patients suffered different lesions to the visual cortex at different ages, but for the large majority in adulthood, and two of them had bilateral cortical blindness.…”

“…The phenomenon, referred to as ''affective blindsight'', denotes the uncanny ability of such patients to respond correctly, or above chance level, to emotionally salient visual stimuli presented to their blind fields (Anders et al, 2004(Anders et al, , 2009Bertini, Cecere, & Ladavas, 2013;Cecere, Bertini, Maier, & Ladavas, 2014;de Gelder & Hadjikhani, 2006;de Gelder, Morris, & Dolan, 2005;de Gelder, Pourtois, van Raamsdonk, Vroomen, & Weiskrantz, 2001; de Gelder, Pourtois, & http://dx.doi.org/10.1016/j.concog.2015.05.007 1053-8100/Ó 2015 Elsevier Inc. All rights reserved. Weiskrantz, 2002;de Gelder, Tamietto, Pegna, & Van den Stock, 2014;de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999;Hamm et al, 2003;Heywood & Kentridge, 2000;Morris, DeGelder, Weiskrantz, & Dolan, 2001;Pegna, Khateb, Lazeyras, & Seghier, 2005;Rossion, de Gelder, Pourtois, Guerit, & Weiskrantz, 2000;Tamietto & de Gelder, 2008;Tamietto, Pullens, de Gelder, Weiskrantz, & Goebel, 2012;Tamietto et al, 2009;Van den Stock et al, 2011). As is the case for the original phenomenon of ''blindsight'' (Pöppel, Held, & Frost, 1973;Weiskrantz, Warrington, Sanders, & Marshall, 1974), the ''blind'' component in affective blindsight refers to the patients' statement of not seeing or consciously perceiving the emotional stimuli, while the ''sight'' component reflects their residual ability to respond, discriminate or display spontaneous expressive and physiological responses that are appropriate to the specific emotional content of the visual signals they are presented with.…”

Modulation of cortical excitability can speed up blindsight but not improve it

“…But these phosphenes occurred only when TMS was applied over MT/V5 of both hemispheres or over MT/V5 on the left and V1 on the right. Their existence almost certainly reflects the abnormal hypertrophic connexions between MT/V5 of the blind hemisphere and the normal hemispheres and/or the enhanced connexions between the pulvinar, superior colliculus and amygdala, with their subsequent connexions with cortex, in GY's blind hemisphere as revealed by diffusion tensor imaging (Bridge et al, 2008;Tamietto et al, 2012).…”

Dissociation between Goal-directed and Discrete Response Localization in a Patient with Bilateral Cortical Blindness

“…They are thus ideally placed along the dorsal visual stream known to support "vision for action." Moreover, these areas can receive direct visual input bypassing V1 from the superior colliculus, which also contains bimodal neurons and is directly involved in the control of goal-directed hand movements through monosynaptic connections with cortical and subcortical motor areas as well as with posterior parietal regions (Tamietto, Pullens, de Gelder, Weiskrantz, & Goebel, 2012;Tamietto et al, 2010;. More specifically, there is neuropsychological evidence suggesting a causal role of the posterior parietal cortex in visuomotor localization of targets presented in the hemianopic field of blindsight participants (Danckert et al, 2003).…”