On imputing function to structure from the behavioural effects of brain lesions

Abstract

What is the link, if any, between the patterns of connections in the brain and the behavioural e¡ects of localized brain lesions ? We explored this question in four related ways. First, we investigated the distribution of activity decrements that followed simulated damage to elements of the thalamocortical network, using integrative mechanisms that have recently been used to successfully relate connection data to information on the spread of activation, and to account simultaneously for a variety of lesion e¡ects. Second, we examined the consequences of the patterns of decrement seen in the simulation for each type of inference that has been employed to impute function to structure on the basis of the e¡ects of brain lesions. Every variety of conventional inference, including double dissociation, readily misattributed function to structure. Third, we tried to derive a more reliable framework of inference for imputing function to structure, by clarifying concepts of function, and exploring a more formal framework, in which knowledge of connectivity is necessary but insu¤cient, based on concepts capable of mathematical speci¢cation. Fourth, we applied this framework to inferences about function relating to a simple network that reproduces intact, lesioned and paradoxically restored orientating behaviour. Lesion e¡ects could be used to recover detailed and reliable information on which structures contributed to particular functions in this simple network. Finally, we explored how the e¡ects of brain lesions and this formal approach could be used in conjunction with information from multiple neuroscience methodologies to develop a practical and reliable approach to inferring the functional roles of brain structures.

Organization, development and function of complex brain networks

“…Thus, inter-cluster connections can be of particular importance for the structural stability and efficient working of cortical networks. The degree of CONNECTEDNESS of neural structures can affect the functional impact of local and remote network lesions [43], and this property might also be an important factor for inferring the function of individual regions from lesioninduced performance changes. Indeed, the cortical networks of cat and macaque are vulnerable to the damage of the few highly connected nodes [44] in a similar way that scale-free networks react to the elimination of hubs [45].…”

Motor imagery: A window into the mechanisms and alterations of the motor system

“…Together, these studies provide some support for a role of M1 in motor imagery, although it should be kept in mind that M1 operates within an interconnected cerebral network, and the effects of a perturbation delivered at one node of a network may influence behavior through changes in other nodes. This consideration applies both to TMS studies (Ruff et al, 2006;Strafella and Paus, 2001) and patient studies (Price and Friston, 2002a;Young et al, 2000). Several electrophysiological studies in humans have also involved motor cortex in motor imagery (Caldara et al, 2004;Carrillo-dela-Pena et al, 2006;McFarland et al, 2000;.…”

Operational principles of neurocognitive networks

“…The technique having the longest history in the study of large-scale cortical function is clinical analysis of the functional consequences of focal brain lesions in patients (Broca, 1861;Penfield and Milner, 1958;Luria, 1962Luria, , 1973Lezak, 1995;Kolb, 1999;Young et al, 2000). Beginning in the nineteenth century, clinical studies were supplemented by studies of intentional lesions in animals.…”

“…Diaschisis suggests that the proper functioning of local area networks is through interactions with other connected local area networks (Bressler, 2002;Passingham et al, 2002). In simulation studies (Young et al, 2000), a local network's vulnerability to dysfunction due to a remote lesion depends on its pattern of connectivity within the large-scale network: (a) local networks with relatively few connections have low vulnerability to lesions in other local networks to which they do not directly connect, but very high vulnerability to lesions in those to which they do directly connect; whereas (b) local networks with relatively many connections are less affected by lesions in local networks to which they directly connect, but are more affected by lesions in those to which they do not directly connect. These results suggest that the function of a local area network depends on its pattern of synaptic interconnectivity with other local networks.…”