Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements

Isomura, Yoshikazu; Harukuni, Rie; Takekawa, Takashi; Aizawa, Hidenori; Fukai, Tomoki

doi:10.1038/nn.2431

Cited by 199 publications

(264 citation statements)

References 46 publications

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“…Together with the mean PSTHs, this means that both classes of neurons show substantial cross-condition modulation, but cross-condition modulation was stronger for narrow-spiking neurons and their firing rates were more likely to increase than decrease. This contrasts sharply with results from rat forelimb motor cortex, in which interneurons show cross-condition modulation almost exclusively during the movement epoch and show little tuning for movement direction (Isomura et al 2009). Merchant et al (2008), however, found a generally similar pattern of firing rate changes in monkey primary motor cortex.…”

Section: # Of Neuronscontrasting

confidence: 96%

“…A recent study examined whether an oculomotor-like output-gating mechanism might be at play in forelimb movements in rats (Isomura et al 2009). They found evidence against such a mechanism, but they also note that rats do not have a clear PMd-M1 separation and found that interneurons were only weakly tuned, in contrast to known interneuron tuning in monkey M1 (Merchant et al 2008).…”

Section: Introductionmentioning

confidence: 99%

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Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Kaufman

Churchland

Santhanam³

et al. 2010

Journal of Neurophysiology

130

134

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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.

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Section: # Of Neuronscontrasting

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Kaufman

Churchland

Santhanam³

et al. 2010

Journal of Neurophysiology

130

134

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“…Neurons in the present study were classified as RS, FS, or "unspecified" based on analysis of their extracellular spiking features, but only RS and FS neurons were included in this analysis. Combined morphological and physiological studies have revealed that in most instances RS and FS neurons may be reliably identified as pyramidal neurons and inhibitory interneurons, respectively (McCormick et al, 1985;Rao et al, 1999;Tanaka, 1999;Compte et al, 2000;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Isomura et al, 2009). "Baseline firing rate" was defined as the average firing rate recorded from a neuron when the animal was sitting quietly.…”

Section: Methodsmentioning

confidence: 99%

“…Recent studies have distinguished spiny (excitatory) and nonspiny (inhibitory) neurons based on characteristics of extracellular spikes (McCormick et al, 1985;Kawaguchi, 1995;Cauli et al, 1997;Rao et al, 1999;Compte et al, 2000;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Isomura et al, 2009). Studies investigating functional interactions between fast-spiking (FS, interneuron) and regular-spiking (RS, pyramidal) neurons in motor and nonmotor areas of cerebral cortex have shown that the incidence of these interactions can vary between different neuronal subtypes (Rao et al, 1999;Tanaka, 1999;Compte et al, 2000;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Merchant et al, 2008;Isomura et al, 2009). Again, similar studies are yet to be performed during different behaviors.…”

Section: Introductionmentioning

confidence: 99%

Differential Involvement of Excitatory and Inhibitory Neurons of Cat Motor Cortex in Coincident Spike Activity Related to Behavioral Context

Putrino

Brown²,

Mastaglia³

et al. 2010

Journal of Neuroscience

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To assess temporal associations in spike activity between pairs of neurons in the primary motor cortex (MI) related to different behaviors, we compared the incidence of coincident spiking activity of task-related (TR) and non-task-related (NTR) neurons during a skilled motor task and sitting quietly in adult cats (Felis domestica). Chronically implanted microwires were used to record spike activity of MI neurons in four animals (two male and two female) trained to perform a skilled reaching task or sit quietly. Neurons were identified as TR if spike activity was modulated during the task (and NTR if not). Based on spike characteristics, they were also classified as either regular-spiking (RS, putatively excitatory) or fast-spiking (FS, putatively inhibitory) neurons. Temporal associations in the activities of simultaneously recorded neurons were evaluated using shuffle-corrected cross-correlograms. Pairs of NTR and TR neurons showed associations in their firing patterns over wide areas of MI (representing forelimb and hindlimb movements) during quiet sitting, more commonly involving RS neurons. During skilled task performance, however, significantly coincident firing was seen almost exclusively between TR neurons in a smaller part of MI (representing forelimb movements), involving mainly FS neurons. The findings of this study show evidence for widespread interactions in MI when the animal sits quietly, which changes to a more specific and restricted pattern of interactions during task performance. Different populations of excitatory and inhibitory neurons appear to be synchronized during skilled movement and quiet sitting.

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“…Compared with primates, rodents in head-fixed conditions are more amenable to state-of-the-art physiological techniques such as intracellular/whole cell recordings (Brecht et al 2004;Crochet and Petersen 2006;Fee 2000;Harvey et al 2009), juxtacellular recording (de Kock and Sakmann 2009;Houweling and Brecht 2008;Isomura et al 2009), multiphoton laserscanning microscopy (Dombeck et al 2007;Komiyama et al 2010), and optogenetic manipulation (Hira et al 2009;Matyas et al 2010). Indeed, there are an increasing number of studies employing rats or mice under head fixation, many of which introduce licking with the tongue Houweling and Brecht 2008;Komiyama et al 2010;Narumi et al 2007;Ono et al 1985;Stüttgen et al 2006;Stüttgen and Schwarz 2008;Welsh et al 1995) or whisking (Bermejo et al 1996(Bermejo et al , 2004Hentschke et al 2006;O'Connor et al 2010aO'Connor et al , 2010b as motor responses in conditional behavior tasks.…”

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confidence: 99%

Reinforcing operandum: rapid and reliable learning of skilled forelimb movements by head-fixed rodents

Kimura

Saiki

Fujiwara-Tsukamoto

et al. 2012

Journal of Neurophysiology

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Isomura Y. Reinforcing operandum: rapid and reliable learning of skilled forelimb movements by head-fixed rodents. J Neurophysiol 108: 1781-1792, 2012. First published June 27, 2012 doi:10.1152/jn.00356.2012.-Stereotaxic head fixation plays a necessary role in current physiological techniques, such as in vivo whole cell recording and two-photon laserscanning microscopy, that are designed to elucidate the cortical involvement in animal behaviors. In rodents, however, head fixation often inhibits learning and performance of behavioral tasks. In particular, it has been considered inappropriate for head-fixed rodents to be operantly conditioned to perform skilled movements with their forelimb (e.g., lever-press task), despite the potential applicability of the task. Here we have solved this problem conceptually by integrating a lever (operandum) and a rewarding spout (reinforcer) into one Љspout-leverЉ device for efficient operant learning. With this device, head-fixed rats reliably learned to perform a pull manipulation of the spout-lever with their right forelimb in response to an auditory cue signal (external-trigger trial, namely, Go trial) within several days. We also demonstrated stable whole cell recordings from motor cortex neurons while the rats were performing forelimb movements in external-trigger trials. We observed a behavior-related increase in the number of action potentials in membrane potential. In the next session, the rats, which had already learned the external-trigger trial, effortlessly performed similar spout-lever manipulation with no cue presentation (internal-trigger trial) additionally. Likewise, some of the rats learned to keep holding the spout-lever in response to another cue signal (No-go trial) in the following session, so that they mastered the Go/No-go discrimination task in one extra day. Our results verified the usefulness of spout-lever manipulation for behavioral experiments employing cutting-edge physiological techniques. rat; operant learning; in vivo whole cell recording

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Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements

Cited by 199 publications

References 46 publications

Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Differential Involvement of Excitatory and Inhibitory Neurons of Cat Motor Cortex in Coincident Spike Activity Related to Behavioral Context

Reinforcing operandum: rapid and reliable learning of skilled forelimb movements by head-fixed rodents

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