The impact of attention on the neuronal mechanisms of adaptation in humans and animals

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Brain neurons adapt or change their responsiveness following the repetition of an environmental event, such as the voice or face of an individual. Neuronal adaptation/repetition effects are thought to be important because a reduced response could indicate familiarity with an individual that we have just met and help cognitive processes to recognize and remember the individual. The neuronal mechanisms of adaptation are of great interest but remain controversial.Human functional magnetic resonance imaging (fMRI) is a non-invasive technique that is increasingly being harnessed to make inferences about neuronal responses during adaptation. Neuronal level study in animal models is required to clarify the neuronal mechanisms. However, although a number of animal neuronal studies of adaptation have shown that neurons generally reduce their firing rates to all stimuli (what is called the ‘response-fatigue’ model of adaptation), the latest human fMRI adaptation studies suggest that this perspective is incomplete. The human results indicate that certain brain regions might contain neurons that can become more selective to specific stimuli or their features after adaptation (what is called the ‘sharpened selectivity’ model). In any case, several scientific issues appear to have complicated the interpretation of the fMRI adaptation response. Namely, the impact of attention has not been studied in the same way in both species, inconsistent experimental paradigms have been used to obtain the human and animal adaptation results, and it is not clear whether the mechanisms of adaptation (which have primarily been studied in the visual system) would be comparable to those in another sensory system, such as the auditory. Therefore, despite the importance of the popular fMRI adaptation phenomenon, the neuronal mechanisms that support it remain highly controversial.This project is designed to address this controversy by implementing a human and animal fMRI project based on the same attentionally-controlled experiment, combined with precisely targeted neuronal recordings in the animals. Specifically, we aim to: 1) evaluate whether fMRI adaptation responses are comparable in humans and animals by conducting the same attentional experiment with both species; 2) extend the latest human fMRI adaptation paradigms to the work with animals, especially the new paradigms that appear to be able to reveal regional changes in neuronal selectivity; and 3) precisely target for neuronal recordings regions showing changes in selectivity and/or those consistent with the response-fatigue model in the animals. Moreover, we aim to conduct the experiment in the visual and auditory modalities (using, respectively, faces or voices as stimuli) to address the correspondence of fMRI adaptation responses across different sensory modalities. This is an important secondary objective because electrophysiological studies have obtained auditory adaptation results in various animals that may or may not be comparable to adaptation in the visual modality of animals. Lastly, although it is not critical for the success of the project, we have the opportunity here to combine fMRI and electrophysiology in animals to be able to more directly associate the fMRI signal and neuronal responses. If successful, our UK institution would be only the second institution in the world to achieve this in conscious behaving animals.In summary, it has become crucial to test the link between human and animal adaptation results by using the same experiment (and stimuli) based on an attentionally controlled task. Our project has the potential to greatly advance our understanding of the neuronal mechanisms of fMRI adaptation and how they might be influenced by or interact with cognitive processes such as those of attention. The results are likely to guide future efforts that employ fMRI adaptation to influence mental processes, including memory and expectancy.