Motor-Related Signals in the Intraparietal Cortex Encode Locations in a Hybrid, rather than Eye-Centered Reference Frame

0 Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College , Hanover, NH 03755, USA 1 Center for Cognitive NeuroscienceDuke University , Durham, NC 27708, USA 2 Brain Imaging and Analysis Center, Duke University , Durham, NC 27707, USA 3 The Author 2008. Published by Oxford University Press. All rights reserved. For permissions , please 4 Department of Neurobiology, Duke University , Durham, NC 27708, USA 5 Department of Psychology and Neuroscience The reference frame used by intraparietal cortex neurons to encode locations is controversial. Many previous studies have suggested eye-centered coding, whereas we have reported that visual and auditory signals employ a hybrid reference frame (i.e., a combination of head- and eye-centered information) (Mullette-Gillman et al. 2005). One possible explanation for this discrepancy is that sensory-related activity, which we studied previously, is hybrid, whereas motor-related activity might be eye centered. Here, we examined the reference frame of visual and auditory saccaderelated activity in the lateral and medial banks of the intraparietal sulcus (areas lateral intraparietal area [LIP] and medial intraparietal area [MIP]) of 2 rhesus monkeys. We recorded from 275 single neurons as monkeys performed visual and auditory saccades from different initial eye positions. We found that both visual and auditory signals reflected a hybrid of head- and eye-centered coordinates during both target and perisaccadic task periods rather than shifting to an eye-centered format as the saccade approached. This account differs from numerous previous recording studies. We suggest that the geometry of the receptive field sampling in prior studies was biased in favor of an eye-centered reference frame. Consequently, the overall hybrid nature of the reference frame was overlooked because the non--eye-centered response patterns were not fully characterized. Introduction The intraparietal cortex is implicated in the processing of spatial information and likely plays a role in guiding attention to, remembering, and responding to the locations of sensory stimuli (for reviews, see Andersen and Gnadt 1989; Colby and Goldberg 1999). The frame of reference of signals in the intraparietal cortex is currently a matter of controversy. Here, we define frame of reference operationally to mean the body part relative to which the response fields show the best alignment. For example, in an eye-centered reference frame, the response fields maintain a consistent position with respect to the direction of the eyes as they move with respect to the head, whereas in a head-centered reference frame (In the present study, the head is immobilized with respect to the world. Thus, head-, body- and world-centered reference frames are all stable with respect to each other in our experiments. For convenience, we will refer to this collection of potential reference frames as head centered.), the response fields maintain a consistent position with respect to the head irrespective of eye movements. This definition is agnostic about potential changes in the magnitude of the response at different fixation positions. Several recording studies have demonstrated that visual signals are heavily influenced by eye position (e.g., Andersen and Mountcastle 1983; Andersen et al. 1985, 1990; Batista et al. 1999) but have described the reference frame as predominantly eye centered despite this eye position influencein other words, these studies have suggested that the response fields align in an eye-centered reference frame and that only the response magnitude (i.e., gain) varies at different eye positions. Related studies involving the double step paradigm have investigated visual and visual memory response patterns before and after the eyes move to a new location. The findings from these studies have been described as being consistent with an eye-centered reference frame that is updated when the eyes move (Duhamel et al. 1992; Colby et al. 1995). Similarly, microstimulation studies in head-unrestrained animals have found that saccades evoked by electrically activating the intraparietal cortex have a constant direction and amplitude with respect to the eye, regardless of initial eye position, again suggesting an eye-centered reference frame (Constantin et al. 2007; see also Thier and Andersen 1998). In contrast, we recently obtained results that were inconsistent with a predominantly eye-centered reference frame in the intraparietal cortex. We investigated visual sensory signals by sampling slices of the response fields for multiple fixation positions (Mullette-Gillman et al. 2005; see also Snyder 2005). Our analysis method focused on the alignment of the response fields, setting aside any potential gain modulations. We reported that the reference frames of individual neurons ranged from predominantly eye centered to predominantly head centered, with most neurons reflecting an intermediate, or hybrid, reference frame in which the neural discharge patterns were not uniquely determined by target location in any single, pure reference frame. We observed a similar pattern for auditory signals, consistent with previous results (Stricanne et al. 1996). In this study, we explore possible explanations for these conflicting findings. Experimentally, we consider the possibility that we missed eye-centered activity by focusing on sensoryrelated activity in our previous study. Accordingly, in this study, we focus on the motor-related activity in LIP. Motor-related activity might be a better measure of what each individual neuron votes for during the read out process. We investigated the motor-related representation of visual and auditory targets in lateral and medial intraparietal neurons in monkeys performing a delayed saccade task. We found that both visual and auditory reference frames continue to be encoded in a hybrid reference frame at the time of the movement, just as they are during the sensory response period. Given our failure to find evidence for a predominantly eye-centered representation in the intraparietal cortex in either the sensory- or motor-related activity periods, we consider other explanations. We reevaluate numerous prior studies and conclude that the geometry of how the response fields were sampled may have biased these studies results to favor eye-centered coordinates. We concur with previous studies that eye position interacts with visual signals to produce response patterns in the intraparietal cortex that are not dictated strictly by the pattern of illumination on the retina (Andersen et al. 1985, 1990; Batista et al. 1999; Cohen and Andersen 2000), but we conclude that the resulting representation includes eye-centered, head-centered, and hybridresponse patterns. Materials and Methods The neuronal data set described here has been the subject of a previous study (Mullette-Gillman et al. 2005). In brief, 275 neurons from the ri (...truncated)