Top-down and bottom-up selective mechanisms in attention: subcortical convergence in visual thalamus?

If a lime gets amongst the lemons at a supermarket fruit stall, it's easily spotted. But a rogue satsuma nestling amidst the clementines is less easily detected, and a novice stock-keeper might need it to be physically pointed out, before he can see it. These are simple examples of two converse ways in which we select an item deserving of attention, referred to by psychologists as 'bottom-up and 'top-down', respectively. In the first example the conspicuous quality of the misplaced lime is termed 'salience'. No property (e.g. 'green' or 'oval shaped') is inherently salient , it all depends on context. In Piccadilly Circus, where everything is designed to be salient, nothing really dominates - giving the sensation of being visually overwhelmed, and not knowing where to look first. In this situation, a 'top-down' instruction - a pointing cue, or a verbal command, can be rather helpful. Redirecting gaze is the typical expression of visual attention, but is not automatic. The focus of attention - the mind's eye - may rove about whilst gaze is frozen (as in social groupings, to avoid eye contact). Attention thus precedes an eye movement, and our aim is to study exactly what happens in the brain at this formative stage. We propose to do this by recording neural activity in the thalamus, a brainstem organ generally responsible for regulating the traffic of sensory information amongst different areas of the cerebral cortex (the brain's top level of information processing). As a strategy, this could be likened to studying the operation of a TV broadcast controlroom, as it covers, say, a Formula 1 Grand Prix. The controlroom receives multiple feeds from all over the racecourse, and the TV-director selects the most dramatic action for transmission to the viewing public. In the terms of this analogy, the thalamus (and in particular a component known as the 'pulvinar') assesses feeds from multiple areas of cerebral cortex - some describing events as they occur, others predicting such events. However, the pulvinar's 'viewing public' is nothing other than the set of cortical areas that provide its input. In other words, the pulvinar is in two-way communication with the cerebral cortex, and acts as a device enabling cortical areas to vote amongst themselves which visible item is the most attention-worthy. Attention is absent under anaesthesia, so we plan to record thalamic activity from an alert, nonhuman primate (NHP). The animal is confronted with an array of items and trained to select the salient item, or a non-descript one that has been pointed out by a suitable visual cue. A neuron in the thalamus, like other visual centres, has a restricted 'receptive field' (RF) - it scrutinises a certain window in the field of view. We locate the RF of a neuron under study, and arrange that it contains the salient, or cued item. Next trial, the target item may be elsewhere. We seek to find neural activity that corresponds to the behavioural significance of the item within the RF, independent of its particular visual features. The timing of activity may vary between the experimentally arranged bottom-up and top-down circumstances and especially, also, between thalamic subdivisions that are differentially connected to bottom-up and top-down cortical pathways. There is another twist to the strategy. We adjust the level of difficulty of the task and monitor how well the NHP performs. It may take longer to reach a decision, or begin to make mistakes. Changes in activity are calibrated against accuracy of performance, to index the dependency of behaviour on specific neural activity. Finally, we can also apply artificial pharmacological stimulation or inhibition to the test site to see if we can influence the selection of the item in its RF - will these artificial manipulations change behavior in line with predictions furnished by neural recordings?

The LGN may differentially amplify selective features of the visual image. In the pulvinar, a 2nd-order thalamic nucleus, cortical inputs replace retinal ones. A signature characteristic - the 'replication principle' - is that reciprocally linked pairs of cortical areas are also enabled to connect indirectly via the pulvinar. If direct intercortical links are adept at feature information transfer, the pulvinar may act to regulate transcortical traffic. Neural models of attention posit a competitive process between rival visible items. Since each item is represented across multiple areas of cortex, a mechanism is inferred to ensure that the dominant activation in each area does not derive from different items - to avert a fragmented, rather than focused state of attention. The project asks if the pulvinar and LGN together are instrumental in so coordinating cortical activity. Automatic bottom-up mechanisms of spatial selection will be contrasted with top-down selection mediated by a symbolic cue. NHPs will be trained to select a salient item, or a cued item from an array of distractors, and we shall look for a neuro-behavioural correlate between psychophysical task performance over a range of difficulty, and concurrently recorded thalamic activity. We shall also apply pharmacologically mediated stimulation and inhibition to the test site, to test the predicted effects upon task performance. We also aim to distinguish the functions of the dorsal and ventral pulvinar subdivisions (DP and VP). DP is directly linked to a fronto-parietal attention control network, VP to the ventral pathway for object analysis - associating DP and VP with cued or salience driven mechanisms respectively. DP and VP do not communicate directly, but indirect circuits exist to transfer salience and cue information between them. The nature of the circuitry thus predicts the relative timing of top-down and bottom-up attentional mechanisms within DP and VP, and between pulvinar and LGN.