Functional reorganisation and recovery following cortical lesions: A preliminary study in macaque monkeys

Abstract

Damage following traumatic brain injury or stroke can often extend beyond the boundaries of the initial insult and can lead to maladaptive cortical reorganisation. On the other hand, beneficial cortical reorganisation leading to recovery of function can also occur. We used resting state FMRI to investigate how cortical networks in the macaque brain change across time in response to lesions to the prefrontal cortex, and how this reorganisation correlated with changes in behavioural performance in cognitive tasks. After prelesion testing and scanning, two monkeys received a lesion to regions surrounding the left principal sulcus followed by periodic testing and scanning. Later, the animals received another lesion to the opposite hemisphere and additional testing and scanning. Following the first lesion, we observed both a behavioural impairment and decrease in functional connectivity, predominantly in frontal-frontal networks. Approximately 8 weeks later, performance and connectivity patterns both improved. Following the second lesion, we observed a further behavioural deficit and decrease in connectivity that showed little recovery. We discuss how different mechanisms including alternate behavioural strategies and reorganisation of specific prefrontal networks may have led to improvements in behaviour. Further work will be needed to confirm these mechanisms.

Combining Brain Perturbation and Neuroimaging in Non-human Primates

“…Interhemispheric reorganisation was also observed in a longitudinal study of two monkeys with lesions to the dorsolateral prefrontal cortex (dlPFC) (Ainsworth et al, 2018). After a unilateral lesion to the left principal sulcus, functional connectivity of frontal regions was transiently disrupted, before restoration of close-to-normal connectivity 8-weeks post-damage.…”

“…After a unilateral lesion to the left principal sulcus, functional connectivity of frontal regions was transiently disrupted, before restoration of close-to-normal connectivity 8-weeks post-damage. However, after a further unilateral lesion to the principal sulcus in the opposite hemisphere, functional connectivity in frontal regions was permanently disrupted, with a concurrent increase in fronto-parietal connectivity, which may represent compensatory plasticity (Ainsworth et al, 2018). The lesions furthermore affected visuospatial and non-spatial working memory, with some recovery of function that may reflect the observed changes in functional connectivity.…”

Frontopolar cortex is a mediator of network modularity in the primate brain

“…This further suggests that even after several years, plasticity such that it exists is insufficient to return the network to a nearly normal state. Hence the effects of FPC lesions on extended brain networks may be robust for several years (and although our data cannot speak to longer periods than 40 months, 40 months appears to be a long time in terms of brain plasticity and recovery of function, especially in light of our own previous studies of functional recovery after frontal lesions in macaques 33 , so it is not unreasonable to predict that FPC-lesion mediated changes to brain network structure may indeed extend to decades or even to the lifetime).…”

“…Finally, functional connectivity was estimated by calculating pairwise correlation coefficients (Pearson's r) for each pair of CC areas (260 areas, 130 in each hemisphere) and transformed using Fisher's r-to-z transform. For further details of the pre-processing of structural images & resting state data see Ainsworth et al, 2018& Mitchell et al, 2016 33,54 .…”

Perceived ambiguity of social interactions increases coupling between frontal and temporal nodes of the social brain

“…Proton-density weighted images using a gradient-refocused echo (GRE) sequence (TR=10 ms, TE= 2.52 ms, flip angle= 25) were acquired as reference for body motion artefact correction during pre-processing. T1-weighted MP-RAGE images (0.5x0.5x0.5 mm resolution, TR = 2,500 ms, TE = 4.01 ms, 3-5 sequences per image) were acquired from each of the three monkeys in separate scanning sessions and were collected under general anaesthesia (see (Ainsworth et al, 2018;Mitchell et al, 2016) for further details of anaesthesia protocols and T1 image acquisition).…”