Idiosyncratic and systematic aspects of spatial representations in the macaque parietal cortex

Abstract

The sensorimotor transformations for visually guided reaching were originally thought to take place in a series of discrete transitions from one systematic frame of reference to the next with neurons coding location relative to the fixation position (gaze-centered) in occipital and posterior parietal areas, relative to the shoulder in dorsal premotor cortex, and in muscle-or jointbased coordinates in motor output neurons. Recent empirical and theoretical work has suggested that spatial encodings that use a range of idiosyncratic representations may increase computational power and flexibility. We now show that neurons in the parietal reach region use nonuniform and idiosyncratic frames of reference. We also show that these nonsystematic reference frames coexist with a systematic compound gain field that modulates activity proportional to the distance between the eyes and the hand. Thus, systematic and idiosyncratic signals may coexist within individual neurons.gain field | posterior parietal cortex | reference frame transformation W e are currently at a theoretical crossroads regarding how the brain computes motor commands from sensory information. The linear systems engineering tradition taught that neural circuits are assembled to compute particular transfer functions and that intermediate stages represent quantities with straightforward physical interpretations (1). At each stage, neurons encode information in a single frame of reference, which facilitates simple pooling. Each cell has a unique receptive field or preferred direction. This results in a distributed population code where each neuron encodes similar information in a similar manner. The vestibular-ocular reflex provides an example of this approach. Head rotation, measured by the vestibular semicircular canals using a canal-centered frame of reference, was believed to be transformed directly into oculomotor commands by virtue of appropriate synaptic weights on vestibular and oculomotor nuclei neurons (1). Visually guided reaching provides another example. Visual spatial information was originally thought to undergo a series of discrete transformations from a sensory (gaze-centered) frame of reference in the occipital and parietal cortices to hand-centered in the premotor cortex (extrinsic motor coordinates) and finally, to muscle commands in the primary motor cortex (intrinsic motor commands) (2-6). The parietal reach region (PRR) in the posterior parietal cortex (PPC) was seen as a discrete processing stage in which reachrelated spatial information was encoded using a uniform gazecentered reference frame and passed on to dorsal premotor cortex (PMd) (7,8).An alternative design borrows from connectionist principles and the field of artificial intelligence. In a trained neural network, the organizational principles may be obscure and individual nodes may encode information idiosyncratically (9, 10). Flexibility and computational power are increased when individual nodes code diverse, seemingly random permutations of the input. Subsequent processing ...

Temporal Analysis of Reference Frames in Parietal Cortex Area 5d during Reach Planning

“…Instead we found that hand position is in fact coded relative to gaze location at this point in the task, possibly reflecting the immediate behavioral goal of maintaining hand and gaze fixation. The source of this signal could be the PRR or PMd, both of which have similar HϪG encoding during the fixation period (Chang et al, 2009;Pesaran et al, 2010, their supplemental material). The HϪG signal is not maintained throughout the task, but becomes progressively weaker in the population once the reach target is present and the behavioral goal is shifted toward planning the upcoming reach.…”

“…This is in contrast to neighboring PRR where cells usually show a clear cue-related peak, followed by sustained firing during the delay period (see Cui and Andersen, 2011, Figure 3, for examples of population responses for PRR and area 5d). PRR has been found to code reach targets in a predominantly gaze-centered reference frame Batista et al, 1999;Buneo et al, 2002;Cohen and Andersen, 2002;Pesaran et al, 2006, but see Mullette-Gillman et al, 2005Chang and Snyder, 2010;McGuire and Sabes, 2011). There is no a priori reason why cells that code an upcoming reach movement relative to the direction of gaze should also have visually evoked responses.…”

“…Despite some heterogeneity among individual cells (Avillac et al, 2005;Chang and Snyder, 2010;McGuire and Sabes, 2011), identified subregions in posterior parietal cortex appear to code in distinct and systematic reference frames. For example, in the parietal reach region (PRR) the target is represented predominantly in a gaze-centered reference frame Batista et al, 1999;Buneo et al, 2002;Cohen and Andersen, 2002;Pesaran et al, 2006), whereas the dorsal aspect of area 5 (area 5d) shows positional tuning during stationary posture (Georgopoulos et al, 1984;Lacquaniti et al, 1995) and codes upcoming targets mainly in a hand-centered reference frame (Bremner and Andersen, 2012).…”

Functional Rather than Effector-Specific Organization of Human Posterior Parietal Cortex

“…This calculation must be based on an estimate of the body's current posture and requires an alignment of the reference frames involved in visual processing and limb movement planning. Whereas saccade planning is thought to occur in eye-centered coordinates, both eye-and body-related reference frames are probably used for limb movement planning (Pesaran et al, 2006;Chang and Snyder, 2007;Marzocchi et al, 2008;Chang et al, 2009;Ferraina et al, 2009;McGuire and Sabes, 2009;Bernier and Grafton, 2010;Chang and Snyder, 2010;Pesaran et al, 2010). The PPC, and especially the SPL, has been suggested to play a major role in the estimation of the current limb positions using proprioceptive and visual information (Graziano et al, 2000;Shadmehr and Krakauer, 2008;Jackson et al, 2009), implicated, for example, by patients suffering from optic ataxia (Karnath and Perenin, 2005).…”

Dissociating contributions of head and torso to spatial reference frames: The misalignment paradigm

“…Sensory systems are known to process information in frames of reference anchored to specific body-parts (e.g., Graziano, Yap, & Gross, 1994), as well as hybrid frames involving combinations of these (e.g., Carrozzo & Lacquaniti, 1994), and idiosyncratic frames for transformation between body-part anchored frames (e.g., Chang & Snyder, 2010;Gazzaniga, Ledoux, & Wilson, 1977). Though frames of reference of this kind are often called 'egocentric', some are keen to distinguish this range of body-part anchored coding from the 'egocentric' structure of perceptual experience (Brewer & Pears, 1993;Foley et al, 2015;Levinson, 1996).…”