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The Journal of Neuroscience, June 9, 2004, 24(23):5356-5363; doi:10.1523/JNEUROSCI.4587-03.2004

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Behavioral/Systems/Cognitive
Rapid Prefrontal-Hippocampal Habituation to Novel Events

Shuhei Yamaguchi,^1,2 Laura A. Hale,² Mark D'Esposito,² and Robert T. Knight²

¹Department of Neurology, Shimane University School of Medicine, Izumo 693-8501, Japan, and ²Department of Psychology, Henry H. Wheeler Jr Brain Imaging Center, and Helen Wills Neuroscience Institute, University of California at Berkeley, Berkeley, California 94720-1650

Unexpected novel events generate an orienting response that plays an important role in some forms of learning and memory. The orienting response involuntarily captures attention and rapidly habituates as events become familiarized. Although evidence from patients with focal lesions and scalp and intracranial event-related brain potential recordings supports the involvement of a distributed neural network involving association cortex and the limbic system in novelty detection, the key neural substrates and temporal dynamics have not been defined. While subjects performed a bi-field visual-selective attention task with random novel stimuli embedded in either attended or unattended visual fields, we measured rapid changes of regional blood oxygenation level-dependent (BOLD) signal to target and novel stimuli using single-trial analysis of event-related functional magnetic resonance imaging with a 4T scanner. Habituation was quantified by serial BOLD signal changes during the first 10 novel stimuli for each subject. Novel stimuli activated the bilateral superior/middle frontal gyrus, temporal-parietal junction, superior parietal lobe, cingulate gyrus, hippocampus, and fusiform gyrus. The superior/middle frontal gyrus and hippocampus showed significant reduction of BOLD signal during the first few novel stimuli, whereas the signals in the fusiform and cingulate gyrus were constant. Prefrontal and hippocampal responses to attended and unattended novel stimuli were comparably habituated. These results, and previous data from lesion studies, support the view that prefrontal and hippocampal regions are involved in rapid automatic detection and habituation to unexpected environmental events and are key elements of the orienting response in humans.

Key words: orienting response; novelty detection; event-related fMRI; single trial analysis; visual attention; limbic system

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Received Oct 10, 2003; revised April 29, 2004; accepted April 29, 2004.

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