Biophysical Support for Functionally Distinct Cell Types in the Frontal Eye Field

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Cohen JY, Heitz RP, Schall JD, Woodman GF. On the origin of event-related potentials indexing covert attentional selection during visual search. J Neurophysiol 102: 2375-2386. First published August 12, 2009 doi:10.1152/jn.00680.2009. Despite nearly a century of electrophysiological studies recording extracranially from humans and intracranially from monkeys, the neural generators of nearly all human event-related potentials (ERPs) have not been definitively localized. We recorded an attention-related ERP component, known as the N2pc, simultaneously with intracranial spikes and local field potentials (LFPs) in macaques to test the hypothesis that an attentional-control structure, the frontal eye field (FEF), contributed to the generation of the macaque homologue of the N2pc (m-N2pc). While macaques performed a difficult visual search task, the search target was selected earliest by spikes from single FEF neurons, later by FEF LFPs, and latest by the m-N2pc. This neurochronometric comparison provides an empirical bridge connecting macaque and human experiments and a step toward localizing the neural generator of this important attention-related ERP component.The electroencephalogram (EEG) has long been used as an electrophysiological measure of human brain activity (Berger 1929). Time-averaged event-related potentials (ERPs) derived from the EEG map onto diverse perceptual and cognitive states and processes (Rugg and Coles 1995). However, definitively identifying the neural generators of ERP components measuring specific cognitive operations has been intractable because the number of source configurations that can produce a given EEG voltage distribution on the scalp is infinite (Hillyard and Anllo-Vento 1998;Luck 2006;Nunez and Srinivasan 2006). Helmholtz (1853) proved that when the number of electrical generators is unknown, an infinite number of inverse solutions can account for any pattern of voltages across a sphere (like the head). Since the dawn of human electrophysiology, investigators have sought solutions to this inverse problem (Adrian and Matthews 1934;Walter 1938). Modern approaches infer the neural generators of human ERP components using source estimation algorithms (Nunez and Srinivasan 2006) or additional information from brain imaging (e.g., Heinze et al. 1994). However, this basic problem will remain underdetermined without constraints from intracranial recordings.Intracranial recordings from epilepsy patients have provided useful information (Lachaux et al. 2003;Michel et al. 2004), but clinical and ethical constraints limit the general utility of this approach. Intracranial recordings can be carried out systematically and thoroughly in nonhuman primates. However, this is predicated on the homology of specific ERP components in humans and nonhuman primates. Several studies have identified ERP components in monkeys that are homologous to those in humans (Arthur and Starr 1984;Glover et al. 1991;Javitt et al. 1992;Lamme et al. 1992; Mehta et al. 2000a,b;Paller et al. 1992;Schroeder et al. 1991S...

Section: Discussionmentioning

confidence: 99%

On the Origin of Event-Related Potentials Indexing Covert Attentional Selection During Visual Search

Cohen

Heitz

Schall

et al. 2009

Self Cite

“…The FEF contains diverse neurons that can be distinguished functionally, with the majority of neurons exhibiting visual responses and many others associated with saccade preparation (Bruce and Goldberg 1985;DiCarlo and Maunsell 2005;Hanes et al 1998;Helminski and Segraves 2003;Schall 1991;Segraves and Goldberg 1987;Sommer and Wurtz 2001). Recent evidence for biophysical differences among cell types in FEF has been provided (Cohen et al 2009). Neurons with visual responses and presaccadic movement-related activity were distinguished with the conventional memory-guided saccade task (Bruce and Goldberg 1985;Hikosaka and Wurtz 1983) and visual inspection of patterns of modulation before visually guided saccades.…”

Section: Overview Of Physiological Analysesmentioning

confidence: 99%

“…Implicit in the descriptions of most studies describing sensorimotor processing, numerous investigators have described visual, visuomovement, and movement neurons in FEF (Bruce and Goldberg 1985;DiCarlo and Maunsell 2005;Helminski and Segraves 2003;Segraves and Goldberg 1987;Umeno andGoldberg 1997, 2001) and SC (Horwitz and Newsome 1999;Mays and Sparks 1980;McPeek and Keller 2002a) and have identified visual neurons in FEF and SC with visual processing but not saccade programming (Horwitz and Newsome 1999;Horwitz et al 2004;McPeek and Keller 2002b;Sato and Schall 2003;Sato et al 2001;Thompson et al 1996Thompson et al , 1997. In fact, a biophysical correlate of the fundamental neuron types in FEF has been reported (Cohen et al 2009). Data from the stop-signal task show that saccaderelated but not visual activity in FEF and SC can be identified with saccade programming that specifies whether and when saccades will be initiated Paré and Hanes 2003).…”

Section: On the Classification Of Neuron Typesmentioning

confidence: 99%

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Neural Control of Visual Search by Frontal Eye Field: Effects of Unexpected Target Displacement on Visual Selection and Saccade Preparation

Murthy¹,

Ray²,

Shorter³

et al. 2009

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Murthy A, Ray S, Shorter SM, Schall JD, Thompson KG. Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. J Neurophysiol 101: 2485-2506, 2009. First published March 4, 2009 doi:10.1152/jn.90824.2008. The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process-targetstep reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys' response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation. I N T R O D U C T I O NTo investigate the neural basis of the decision processes of saccade target selection, we have recorded neural activity in the frontal eye field (FEF) of macaque monkeys trained to perform visual search tasks (Bichot and Schall 1999; Bichot et al.

“…Because interneurons have briefer action potentials than pyramidal neurons (Connors and Gutnick 1990;McCormick et al 1985), and the extracellular waveform reflects the intracellular waveform (Henze et al 2000), the extracellularly recorded waveform duration can be used to distinguish interneurons from pyramidal neurons with substantial reliability (Bartho et al 2004). This technique has previously been used in primary somatosensory cortex (Simons 1978;Swadlow 2003), prefrontal cortex (Diester and Nieder 2008;Johnston et al 2009;Rao et al 1999;Wilson et al 1994), V4 (Mitchell et al 2007), FEF (Cohen et al 2009), and M1 (Merchant et al 2008).…”

Section: Introductionmentioning

confidence: 99%

Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Kaufman

Churchland

Santhanam³

et al. 2010

129

130

Dorsal premotor cortex (PMd) is known to be involved in the planning and execution of reaching movements. However, it is not understood how PMd plan activity-often present in the very same neurons that respond during movement-is prevented from itself producing movement. We investigated whether inhibitory interneurons might "gate" output from PMd, by maintaining high levels of inhibition during planning and reducing inhibition during execution. Recently developed methods permit distinguishing interneurons from pyramidal neurons using extracellular recordings. We extend these methods here for use with chronically implanted multi-electrode arrays. We then applied these methods to single-and multi-electrode recordings in PMd of two monkeys performing delayed-reach tasks. Responses of putative interneurons were not generally in agreement with the hypothesis that they act to gate output from the area: in particular it was not the case that interneurons tended to reduce their firing rates around the time of movement. In fact, interneurons increased their rates more than putative pyramidal neurons during both the planning and movement epochs. The two classes of neurons also differed in a number of other ways, including greater modulation across conditions for interneurons, and interneurons more frequently exhibiting increases in firing rate during movement planning and execution. These findings provide novel information about the greater responsiveness of putative PMd interneurons in motor planning and execution and suggest that we may need to consider new possibilities for how planning activity is structured such that it does not itself produce movement.