Neural Reorganization Due to Neonatal Amygdala Lesions in the Rhesus Monkey: Changes in Morphology and Network Structure

Abstract

It is generally believed that neural damage that occurs early in development is associated with greater adaptive capacity relative to similar damage in an older individual. However, few studies have surveyed whole brain changes following early focal damage. In this report, we employed multimodal magnetic resonance imaging analyses of adult rhesus macaque monkeys who had previously undergone bilateral, neurotoxic lesions of the amygdala at about 2 weeks of age. A deformation-based morphometric approach demonstrated reduction of the volumes of the anterior temporal lobe, anterior commissure, basal ganglia, and pulvinar in animals with early amygdala lesions compared to controls. In contrast, animals with early amygdala lesions had an enlarged cingulate cortex, medial superior frontal gyrus, and medial parietal cortex. Diffusion-weighted imaging tractography and network analysis were also used to compare connectivity patterns and higher-level measures of communication across the brain. Using the communicability metric, which integrates direct and indirect paths between regions, lesioned animals showed extensive degradation of network integrity in the temporal and orbitofrontal cortices. This work demonstrates both degenerative as well as progressive large-scale neural changes following long-term recovery from neonatal focal brain damage.

Chemogenetic inhibition of the amygdala modulates emotional behavior expression in infant rhesus monkeys

“…In contrast to results obtained after neonatal amygdala lesions on the human intruder task Raper et al, 2013a), the present study in infant monkeys did not exhibit changes in vocalizations and hostile behavior expression after DREADD-mediated amygdala inactivation. The differences between the previous lesion studies and the current study suggest that the more extensive behavioral changes with permanent lesions could be due to lesion-induced plasticity changes after early permanent damage Raper et al, 2014b;Grayson et al, 2017;Payne et al, 2017).…”

“…Given the potential for neural plasticity during this postnatal period, there is considerable opportunity for reorganization and compensation from other brain structures. In fact, several studies have demonstrated how lesions early in life contribute to such reorganization Raper et al, 2014b;Grayson et al, 2017;Payne et al, 2017). In order to avoid the pitfalls of permanent lesions and better address these questions we need tools that transiently activate or inactivate the amygdala during early development.…”

Transient Hypothyroidism During Lactation Arrests Myelination in the Anterior Commissure of Rats. A Magnetic Resonance Image and Electron Microscope Study

“…This is the case of patients who suffer toxic leucoencephalopathy associated with the use of drugs such as opioids and cocaine ( Buttner and Weis, 2006 ; Alturkustani et al, 2017 ) in which demyelination of commissural and white matter axons in the cerebral cortex becomes detectable in MRI scans at an advanced stage of the disease ( Phan-Ba et al, 2012 ). Diffusion image measurements of amygdala-lesioned young monkeys are relatively insensitive to white matter changes during recovery ( Grayson et al, 2017 ). This is relevant since early detection by T2w MRI scans of some neurological and psychiatric diseases that affect myelination of cortical axons, and other important factors may not be possible.…”

Amygdala Represents Diverse Forms of Intangible Knowledge, That Illuminate Social Processing and Major Clinical Disorders

“…Biological motion and multimodal information are processed in superior temporal sulcus (STS; Beauchamp, 2005 ; Pelphrey et al, 2005 ; Saygin, 2007 ), of which predominantly anterior STS relays to amygdala (McDonald, 1998 ; Stefanacci and Amaral, 2000 , 2002 ; Freese and Amaral, 2009 ). These interconnections are further supported by findings that early amygdala lesions in monkey and human result in significant degradation of anterior subregions of VTC and STS (Boes et al, 2012 ; Grayson et al, 2017 ). Auditory inputs from the high-level auditory area, in monkey predominantly area TAa located in superior temporal gyrus (STG), relay to amygdala (McDonald, 1998 ; Stefanacci and Amaral, 2000 , 2002 ; Yukie, 2002 ; Freese and Amaral, 2009 ).…”