Katherine Woollett

Acquiring “the Knowledge” of London's Layout Drives Structural Brain Changes

Summary The last decade has seen a burgeoning of reports associating brain structure with specific skills and traits (e.g., [1–8]). Although these cross-sectional studies are informative, cause and effect are impossible to establish without longitudinal investigation of the same individuals before and after an intervention. Several longitudinal studies have been conducted (e.g., [9–18]); some involved children or young adults, potentially conflating brain development with learning, most were restricted to the motor domain, and all concerned relatively short timescales (weeks or months). Here, by contrast, we utilized a unique opportunity to study average-IQ adults operating in the real world as they learned, over four years, the complex layout of Londons streets while training to become licensed taxi drivers. In those who qualified, acquisition of an internal spatial representation of London was associated with a selective increase in gray matter (GM) volume in their posterior hippocampi and concomitant changes to their memory profile. No structural brain changes were observed in trainees who failed to qualify or control participants. We conclude that specific, enduring, structural brain changes in adult humans can be induced by biologically relevant behaviors engaging higher cognitive functions such as spatial memory, with significance for the “nature versus nurture” debate.

Talent in the taxi: a model system for exploring expertise

While there is widespread interest in and admiration of individuals with exceptional talents, surprisingly little is known about the cognitive and neural mechanisms underpinning talent, and indeed how talent relates to expertise. Because many talents are first identified and nurtured in childhood, it can be difficult to determine whether talent is innate, can be acquired through extensive practice or can only be acquired in the presence of the developing brain. We sought to address some of these issues by studying healthy adults who acquired expertise in adulthood. We focused on the domain of memory and used licensed London taxi drivers as a model system. Taxi drivers have to learn the layout of 25 000 streets in London and the locations of thousands of places of interest, and pass stringent examinations in order to obtain an operating licence. Using neuropsychological assessment and structural and functional magnetic resonance imaging, we addressed a range of key questions: in the context of a fully developed brain and an average IQ, can people acquire expertise to an exceptional level; what are the neural signatures, both structural and functional, associated with the use of expertise; does expertise change the brain compared with unskilled control participants; does it confer any cognitive advantages, and similarly, does it come at a cost to other functions? By studying retired taxi drivers, we also consider what happens to their brains and behaviour when experts stop using their skill. Finally, we discuss how the expertise of taxi drivers might relate to the issue of talent and innate abilities. We suggest that exploring talent and expertise in this manner could have implications for education, rehabilitation of patients with cognitive impairments, understanding individual differences and possibly conditions such as autism where exceptional abilities can be a feature.

Navigational expertise may compromise anterograde associative memory

Grey matter volume increases have been associated with expertise in a range of domains. Much less is known, however, about the broader cognitive advantages or costs associated with skills and their concomitant neuroanatomy. In this study we investigated a group of highly skilled navigators, licensed London taxi drivers. We replicated findings from previous studies by showing taxi drivers had greater grey matter volume in posterior hippocampus and less grey matter volume in anterior hippocampus compared to matched control subjects. We then employed an extensive battery of tests to investigate the neuropsychological consequences of being a skilled taxi driver. Their learning of and recognition memory for individual items was comparable with control subjects, as were working memory, retrograde memory, perceptual and executive functions. By contrast, taxi drivers were significantly more knowledgeable about London landmarks and their spatial relationships. However, they were significantly worse at forming and retaining new associations involving visual information. We consider possible reasons for this decreased performance including the reduced grey matter volume in the anterior hippocampus of taxi drivers, similarities with models of aging, and saturation of long-term potentiation which may reduce information-storage capacity.

Impairments in proverb interpretation following focal frontal lobe lesions

The proverb interpretation task (PIT) is often used in clinical settings to evaluate frontal “executive” dysfunction. However, only a relatively small number of studies have investigated the relationship between frontal lobe lesions and performance on the PIT. We compared 52 patients with unselected focal frontal lobe lesions with 52 closely matched healthy controls on a proverb interpretation task. Participants also completed a battery of neuropsychological tests, including a fluid intelligence task (Raven’s Advanced Progressive Matrices). Lesions were firstly analysed according to a standard left/right sub-division. Secondly, a finer-grained analysis compared the performance of patients with medial, left lateral and right lateral lesions with healthy controls. Thirdly, a contrast of specific frontal subgroups compared the performance of patients with medial lesions with patients with lateral frontal lesions. The results showed that patients with left frontal lesions were significantly impaired on the PIT, while in patients with right frontal lesions the impairments approached significance. Medial frontal patients were the only frontal subgroup impaired on the PIT, relative to healthy controls and lateral frontal patients. Interestingly, an error analysis indicated that a significantly higher number of concrete responses were found in the left lateral subgroup compared to healthy controls. We found no correlation between scores on the PIT and on the fluid intelligence task. Overall our results suggest that specific regions of the frontal lobes contribute to the performance on the PIT.

Non‐spatial expertise and hippocampal gray matter volume in humans

Previous work suggests that spatial expertise in licensed London taxi drivers is associated with differences in hippocampal gray matter volume relative to IQ‐matched control subjects. Here we examined whether non‐spatial expertise is associated with similar hippocampal gray matter effects. We compared medical doctors who, like taxi drivers, acquire a vast amount of knowledge over many years, with IQ‐matched control subjects who had no tertiary education. Whole brain analysis of structural magnetic resonance imaging (MRI) scans using voxel‐based morphometry (VBM) failed to identify any differences in gray matter volume between the groups, including in the hippocampus. Moreover, amount of medical experience that ranged from 0.5 to 22.5 yr did not correlate with gray matter volume in the hippocampus or elsewhere in the brain. We conclude that intensively acquiring a large amount of knowledge over many years is not invariably associated with hippocampal gray matter volume differences. Instead it would seem that hippocampal gray matter volume effects are more likely to be observed when the knowledge acquired concerns a complex and detailed large‐scale spatial layout.

Exploring anterograde associative memory in London taxi drivers

London taxi drivers are renowned for their navigation ability, spending a number of years acquiring ‘The Knowledge’ of London’s complex layout and having to pass stringent examinations to obtain an operating licence. In several studies, this navigation skill has been associated with increased posterior but also decreased anterior hippocampal grey matter volume. Neuropsychologically, gain and loss has also been documented in taxi drivers; while very skilled at navigation in London, they are significantly poorer than controls at learning and recalling new object–location associations. Here we tested a group of London taxi drivers and matched control participants on this object–location associations task, while also subjecting them to a battery of challenging anterograde associative memory tests involving verbal, visual and auditory material both within and across modalities. Our aim was to assess whether their difficulty in previous studies reflected a general problem with associative memory, or was restricted to the spatial domain. We replicated previous findings of poor learning and memory of object–location associations. By contrast, their performance on the other anterograde associative memory tasks was comparable with controls. This resolves an outstanding question in the memory profile of London taxi drivers following hippocampal plasticity, and underlines the close relationship between space and the hippocampus.

The effect of age on cognitive performance of frontal patients

Age is known to affect prefrontal brain structure and executive functioning in healthy older adults, patients with neurodegenerative conditions and TBI. Yet, no studies appear to have systematically investigated the effect of age on cognitive performance in patients with focal lesions. We investigated the effect of age on the cognitive performance of a large sample of tumour and stroke patients with focal unilateral, frontal (n=68), or non-frontal lesions (n=45) and healthy controls (n=52). We retrospectively reviewed their cross sectional cognitive and imaging data. In our frontal patients, age significantly predicted the magnitude of their impairment on two executive tests (Ravens Advanced Progressive Matrices, RAPM and the Stroop test) but not on nominal (Graded Naming Test, GNT) or perceptual (Incomplete Letters) task. In our non-frontal patients, age did not predict the magnitude of their impairment on the RAPM and GNT. Furthermore, the exacerbated executive impairment observed in our frontal patients manifested itself from middle age. We found that only age consistently predicted the exacerbated executive impairment. Lesions to specific frontal areas, or an increase in global brain atrophy or white matter abnormalities were not associated with this impairment. Our results are in line with the notion that the frontal cortex plays a critical role in aging to counteract cognitive and neuronal decline. We suggest that the combined effect of aging and frontal lesions impairs the frontal cortical systems by causing its computational power to fall below the threshold needed to complete executive tasks successfully.