The ‘when’ pathway of the right parietal lobe

The order of events, whether two events are seen as simultaneous or successive, sets the stage for the moment-to-moment interpretation of the visual world. Evidence from patients who have lesions to the parietal lobes and transcranial magnetic stimulation studies in normal subjects suggest that the right inferior parietal lobe underlies this analysis of event timing. Judgment of temporal order, simultaneity and high-level motion are all compromised following right parietal lesions and degraded after transcranial magnetic stimulation over the right parietal but not elsewhere. The results suggest that the right parietal lobe serves as part of a when pathway for both visual fields. We propose that the disruption of this mechanism is the underlying cause of a wide range of seemingly unrelated tasks being impaired in right parietal patients.

Introduction

A central concept in contemporary research is how we identify objects in our visual environment (what) and how we locate those objects (where, or more recently called ‘vision-for-action’) 1, 2. But an equally important ability is how we compute when visual events occur. In the past few years, there has been a growing interest in understanding the psychological and neuronal bases of the temporal dimension in the normally functioning brain and in the neurological population. In addition to behavioral measures and functional imaging studies, several research groups have begun to investigate the mechanisms that register time at the neuronal level 3, 4, 5.

The relative timing of events underlies an enormous range of neural functions, from the microsecond delays of auditory processing to the measure of the seasons. Many theories have been proposed to explain how the brain incorporates time into its computations. In particular, when the timing of two events are separated in space and time beyond the range of classic receptive fields and temporal integration periods, other neural mechanisms must be considered. Some suggest a common neuronal mechanism for all timing operations, from visual to speech perception to timing a wide range of motor tasks (the internal clock model [6]). Others suggest that timing is distributed among different neural structures 7, 8.

Although new insights have been gained into how the temporal processing is performed over short intervals spanning microseconds (e.g. how the sound is localized by the auditory system) to milliseconds (low-level visual motion), the temporal processing at the intermediate level, across intervals up to one second in duration, is probably the most sophisticated form of temporal processing and it is still little studied and poorly understood 9, 10. There are two broad classes of temporal analysis at these longer scales: one that is metric – the judgment of duration or interval between events – and one that is ordinal – the judgment of order of events in a series, a judgment that for some conditions also supports the perception of motion. It is this temporal ordering of events at the intermediate scale, a core element in many cognitive functions, that we address here. We propose that event order at this scale is computed centrally and we report experimental evidence to indicate that this computation is performed in the right parietal lobe in humans.

Much of the work we review investigates judgments of whether two events are simultaneous or whether two events are seen as independent or integrated into the motion of a single object. Patient and transcranial magnetic stimulation (TMS) studies provide evidence for the lateralization of these functions in the brain. In particular, we find that the right parietal lobe has a dominant role in visual time processing of event order at intermediate scales in both visual fields, suggesting that it forms a core structure of a when pathway. The bilateral nature of the control of temporal attention by the right parietal cortex enables us to distinguish spatial and temporal components of attention. For example, the effects of parietal lesions are too variable to fit into a unitary syndrome: controversies continue over localizations of lesions that lead to neglect as well as over lateralization of deficits 11, 12. Here we propose that parietal control over spatial attention is strongly contralateral, whereas the control of the right parietal cortex over temporal attention is bilateral. The difference between bilateral and contralateral effects is then diagnostic of the contributions of spatial and temporal attention in tasks where both are involved. Bilateral deficits in right unilateral parietal lesions ought not to be spatial in nature and, in almost every case where a spatial deficit has been used to explain a bilateral impairment, it can be seen to be confounded by a temporal component.