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

Mullette-Gillman, O'Dhaniel A.; Cohen, Yale E.; Groh, Jennifer M.

doi:10.1093/cercor/bhn207

Cited by 97 publications

(95 citation statements)

References 60 publications

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“…S1A) while monkeys planned and executed reaching movements. Our behavioral task and analyses were designed to identify the frames of reference used by cells in PRR and to distinguish shifts in tuning from gain field effects (30)(31)(32). Making this distinction requires that full tuning functions be obtained (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Making this distinction requires that full tuning functions be obtained (Fig. 1A) (32). To accomplish this efficiently, we aligned a wide target array with each cell's preferred direction to capture the peak and both sides of the tuning function.…”

Section: Resultsmentioning

confidence: 99%

“…33). We revisited this issue using a behavioral paradigm and analysis specifically designed to distinguish shifts in tuning from gain field modulations (30,32). For each cell, we collected full tuning curves, and analyzed the data using a family of nonlinear models with explicit tuning and gain-field terms (Eqs.…”

Section: Discussionmentioning

confidence: 99%

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

Chang

Snyder

2010

Proc. Natl. Acad. Sci. U.S.A.

112

121

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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 ...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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

Chang

Snyder

2010

Proc. Natl. Acad. Sci. U.S.A.

112

121

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“…3) (Mullette-Gillman, Cohen, & Groh, 2005, 2009; Schlack, Sterbing-D’Angelo, Hartung, Hoffmann, & Bremmer, 2005) suggesting an important function in multisensory integration. In that respect, a particularly critical area appears to be VIP.…”

Section: Functional Response Properties: Effector Specificity and Mulmentioning

confidence: 99%

A brief comparative review of primate posterior parietal cortex: A novel hypothesis on the human toolmaker

et al. 2017

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The primate visual system contains two major cortical pathways: a ventral-temporal pathway that has been associated with object processing and recognition, and a dorsal-parietal pathway that has been associated with spatial processing and action guidance. Our understanding of the role of the dorsal pathway, in particular, has greatly evolved within the framework of the two-pathway hypothesis since its original conception. Here, we present a comparative review of the primate dorsal pathway in humans and monkeys based on electrophysiological, neuroimaging, neuropsychological, and neuroanatomical studies. We consider similarities and differences across species in terms of the topographic representation of visual space; specificity for eye, reaching, or grasping movements; multi-modal response properties; and the representation of objects and tools. We also review the relative anatomical location of functionally- and topographically-defined regions of the posterior parietal cortex. An emerging theme from this comparative analysis is that non-spatial information is represented to a greater degree, and with increased complexity, in the human dorsal visual system. We propose that non-spatial information in the primate parietal cortex contributes to the perception-to-action system aimed at manipulating objects in peripersonal space. In humans, this network has expanded in multiple ways, including the development of a dorsal object vision system mirroring the complexity of the ventral stream, the integration of object information with parietal working memory systems, and the emergence of tool-specific object representations in the anterior intraparietal sulcus and regions of the inferior parietal lobe. We propose that these evolutionary changes have enabled the emergence of human-specific behaviors, such as the sophisticated use of tools.

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“…Monkey single-unit recordings have shown that the processing in the PPC involves a mixture of reference frames, including gaze-centered, body-centered, and intermediate coordinates (Stricanne et al, 1996;Avillac et al, 2005;Mullette-Gillman et al, 2005;Chang et al, 2009;Mullette-Gillman et al, 2009;Chang and Snyder, 2010). Recent models suggest that this neural architecture provides the PPC with a mechanism to implicitly create multiple modes of representation at the population level, with each reference frame weighted as a function of global task demands (Pouget et al, 2002;McGuire and Sabes, 2009).…”

Section: Introductionmentioning

confidence: 99%

Multiple Reference Frames in Cortical Oscillatory Activity during Tactile Remapping for Saccades

Buchholz

Jensen²,

Medendorp³

2011

J. Neurosci.

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Single-unit recordings have shown that the brain uses multiple reference frames in spatial processing. The brain could use this neural architecture to implicitly create multiple modes of representation at the population level, with each reference frame weighted as a function of task demands. Using magnetoencephalography, we tested this hypothesis by studying the reference frames in rhythmic neuronal synchronization-a population measure-during tactile remapping for saccades. Human subjects fixated either to the left or right of the body midline, while a tactile stimulus was applied to an invisible fingertip, located either left or right of fixation. After a variable delay, they looked at the remembered stimulus location. Results show a transient body-centered, stimulus-induced gammaband response (70 -90 Hz) in somatosensory areas, contralateral to the stimulated hand. Concurrently, a gamma-band response occurred in posterior parietal cortex (PPC), contralateral to the gaze-centered location of the stimulus, even though the stimulus was not seen. The temporal overlap of these early representations suggests that there is a fast bottom-up sensory-induced remapping in PPC, taking into account the relative positions of eyes and hand. The gaze-centered representation in PPC was sustained in a high gamma range (85-115 Hz) and increased in power closer to the initiation of the saccade. Lower-frequency rhythms (alpha, beta) showed body-centered power modulations in somatosensory areas in anticipation of the stimulus and a mixture of reference frames in PPC after stimulus presentation. We conclude that oscillatory activity reflects the time-varying coding of information in body-and gaze-centered reference frames during tactile remapping for saccades.

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

Cited by 97 publications

References 60 publications

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

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

A brief comparative review of primate posterior parietal cortex: A novel hypothesis on the human toolmaker

Multiple Reference Frames in Cortical Oscillatory Activity during Tactile Remapping for Saccades

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