Evidence for differential top-down and bottom-up suppression in posterior parietal cortex

Koorosh Mirpour James W. Bisley 0 Department of Psychology 1 Jules Stein Eye Institute, David Geffen School of Medicine 2 Department of Neurobiology, David Geffen School of Medicine 3 Brain Research Institute, University of California, Los Angeles , Los Angeles, CA 90095 , USA Articles on similar topics can be found in the following collections Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here References Subject collections Email alerting service rstb.royalsocietypublishing.org Research Cite this article: Mirpour K, Bisley JW. 2013 Evidence for differential top-down and bottom-up suppression in posterior parietal cortex. Phil Trans R Soc B 368: 20130069. http://dx.doi.org/10.1098/rstb.2013.0069 One contribution of 17 to a Theme Issue Attentional selection in visual perception, memory and action. Subject Areas: neuroscience Author for correspondence: James W. Bisley e-mail: Electronic supplementary material is available at http://dx.doi.org/10.1098/rstb.2013.0069 or via http://rstb.royalsocietypublishing.org. Evidence for differential top-down and bottom-up suppression in posterior parietal cortex Koorosh Mirpour1 and James W. Bisley1,2,3,4 When searching for an object, we usually avoid items that are visually different from the target and objects or places that have been searched already. Previous studies have shown that neural activity in the lateral intraparietal area (LIP) can be used to guide this behaviour; responses to task irrelevant stimuli or to stimuli that have been fixated previously in the trial are reduced compared with responses to potential targets. Here, we test the hypothesis that these reduced responses have a different genesis. Two animals were trained on a visual foraging task, in which they had to find a target among a number of physically identical potential targets (T) and task irrelevant distractors. We recorded neural activity and local field potentials (LFPs) in LIP while the animals performed the task. We found that LFP power was similar for potential targets and distractors but was greater in the alpha and low beta bands when a previously fixated T was in the response field. We interpret these data to suggest that the reduced single-unit response to distractors is a bottom-up feed-forward result of processing in earlier areas and the reduced response to previously fixated Ts is a result of active top-down suppression. 1. Introduction Our capacity for processing visual information for perception and action is limited compared with the amount of information that is received by the eye. This makes it necessary to focus our attention on discrete regions of visual space, which is usually done by moving the eye so that gaze centres on the most important objects in the scene. The underlying mechanism driving attentional selection has been studied for years and is thought to be mainly controlled by a parieto-frontal network, which also includes subcortical oculomotor areas [1 4]. It is thought that these areas may function as priority maps, in which features or locations are represented by levels of neural activity related to the attentional priority at that location [5] and which are used to select the focus of both covert and overt attention [6]. In goal-directed behaviour, such as visual search, these priority maps highlight stimuli similar to the target [7 9] and help keep track of where we have looked [10]. Previous studies have shown that neural activity in the lateral intraparietal area (LIP) of posterior parietal cortex can perform both of these functions: responses are greater for task relevant compared with task irrelevant objects [9,11 13] and responses to stimuli that have been fixated during search are reduced [10]. In both cases, the responses to stimuli that are not the target are lower than the responses to the target, however, it is unclear whether these reductions are driven by the same mechanisms. Here, we hypothesize that the reduced response to task irrelevant distractors is a long-term feed-forward result of processing in earlier areas owing to the animals familiarity with the task and stimuli, but that the suppression of items that have been examined previously within the trial is a form of active top-down inhibitory tagging [14,15]. To differentiate between these mechanisms, we examined the local field potential (LFP) activity recorded from LIP while animals performed a visual foraging task. LFP activity is thought to represent both the input and local processing in & 2013 The Author(s) Published by the Royal Society. All rights reserved. response field position but not the output of the recorded area [16,17]. Thus, if the two forms of suppression are owing to two separate mechanisms, they should be distinguishable within the LFP. 2. Material and methods (a) Surgical preparation Two male rhesus monkeys (9 12 kg) were implanted with head posts, scleral coils and recording cylinders during sterile surgery under general anaesthesia; animals were initially anaesthetized with ketamine and xylazine, and maintained with isofluorane (see [10] for details). (b) Electrophysiological recording The experiments were run using the REX system [18] and data were recorded using a Plexon MAP system with an 8-channel Omnetics 0.050 headstage (Plexon Inc., Dallas, TX, USA). Data were analysed using custom code written in MATLAB (Mathworks Inc.) and CHRONUX [19]. Both animals were trained on a standard memory-guided saccade task and the foraging search task (figure 1). We recorded extracellular LFP activity from area LIP using tungsten microelectrodes guided by coordinates from MRI images taken both before and after cylinder implantation. The single-unit activity that was recorded along with LFP activity was reported previously in [20]. Recorded sites were considered to be in LIP if the single-unit activity showed visual, delay and/or peri-saccadic responses during the memoryguided saccade task [21]. After calculating the size and position of the response field for each single neuron (for details see [22]), the foraging task was run and neural data were recorded. Monkeys started each trial of the foraging task by fixating a spot for 450 700 ms. After which, the fixation point was extinguished and an array of potential targets (T) and distractors () was presented, with one where the fixation spot had been (figure 1). One of the Ts had a juice reward associated with it, such that if the monkey looked at it for 500 ms within 8 s after start of trial, he would get the reward. As in previous free-viewing visual search studies [23,24], the stimuli were arranged in such a fashion that when the monkey looked at one stimulus, the response field of the isolated LIP neuron usually encompassed another stimulus. The number of targets and distractors varied in each trial. In most sessions, data were recorded in blocks. In one block, the number of po (...truncated)