Buckley, M. J. | bioRxiv Science

bioRxiv2018

Mnemonic introspection in macaques is dependent on dorsolateral prefrontal but not orbitofrontal cortex

The human prefrontal cortex (PFC) has been associated more with meta-perceptual as opposed to meta-memory decisions from correlational neuroimaging investigations. Recently, metacognitive abilities have also been shown to be causally dependent upon anterior and dorsal PFC in non-human primate lesion studies. Two studies, utilizing post-decision wagering paradigms and reversible inactivation, challenged this meta-perceptual versus meta-memory notion and showed that dorsal and anterior prefrontal areas are associated with metamemory for experienced objects and awareness of ignorance respectively. Causal investigations are important but scarce; nothing is known, for example, about the causal contributions of prefrontal sub-regions to spatial metamemory. Here, we investigated the effects of dorsal versus ventral PFC lesions on two-alternative forced choice spatial discrimination tasks in male macaque monkeys. Importantly, we were rigorous in approach and applied three independent but complementary indices used to quantify individual animals metacognitive ability ("type II sensitivity") namely meta-d', d' measures, and Phi coefficient ({Phi}). Our results were consistent across indices: while neither lesions to superior dorsolateral PFC (sdlPFC) nor orbitofrontal cortex (OFC) impaired spatial recognition performance, only monkeys with sdlPFC lesions were impaired in meta-accuracy. Together with the observation that the same OFC lesioned monkeys were impaired in updating rule-value in a Wisconsin Card Sorting Test analog, we therefore document a functional double-dissociation between these two PFC regions. Out study presents important causal evidence that other dimensions, namely domain-specific processing (e.g., spatial versus non-spatial metamemory), also need considerations in understanding the functional specialization in the neural underpinnings of introspection. Significance StatementThis study demonstrates macaque monkeys meta-cognitive capability of introspecting its own memory success is causally dependent on intact superior dorsolateral prefrontal cortices (PFC) but not the orbitofrontal cortices. Combining neurosurgical techniques on monkeys and state-of-the-art measures of metacognition, we affirm a critical role of the PFC in supporting spatial meta-recognition memory and delineate functional specificity within PFC for distinct elements of metacognition.

neuroscience↗

bioRxiv2017

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

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. Here, we used resting state FMRI (rsFMRI) to examine how functional connectivity in the macaque brain changed across time in response to lesions to the prefrontal cortex, and how this reorganisation correlated with changes in behaviour. Two monkeys were trained to perform location-based and object-based delayed match-to-sample tasks. We also collected rsFMRI data under general anaesthesia at two pre-lesion time-points, separated by 3-4 weeks. After two cycles of testing and scanning, the animals received a principal sulcus lesion followed by an additional 4 cycles of testing and scanning. Later, the same animals received a second lesion to the opposite hemisphere and additional cycles of testing and scanning.\n\nBoth animals showed a marked behavioural impairment following the first lesion, which was associated with a decrease in functional connectivity, predominantly within frontal-frontal networks in both hemispheres. Approximately 8 weeks following the lesion, performance improved, as did functional connectivity within these networks. Following the second lesion, functional connectivity again decreased and this was associated with a marginal behavioural deficit that did not recover.\n\nOur data show that behavioural impairments reflect not just the removal of the lesioned area, but also disturbance to an extensive cortical network. This network can recover by restoring and/or strengthening pre-existing connections, leading to improvement in behaviour.

neuroscience↗