Anticipatory Activity of Motor Cortex in Relation to Rhythmic Whisking

Friedman, Wendy A.; Jones, Lauren M.; Cramer, Nathan; Kwegyir-Afful, Ernest E.; Zeigler, H. Philip; Keller, Asaf

doi:10.1152/jn.00945.2005

Cited by 27 publications

(31 citation statements)

References 31 publications

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“…We have recently reported that increasing ICMS intensity significantly decreases whisking onset latency, most likely by increasing the output from 5-HT premotoneurons , consistent with the postulate that extrasynaptic transmission contributes to the delayed whisking. It is pertinent that the long latencies between cortical activation and EMG onset are consistent with our previous studies in behaving rats (Friedman et al 2006).…”

Section: Discussionsupporting

confidence: 88%

“…Inhibitory inputs are effective in rapidly terminating PICs (Heckman et al 2005), suggesting that inhibitory inputs to vMNs may be involved. Indeed, we have previously found that both the onset and offset of a whisking epoch is preceded by a brief increase in activity in vMCx (Friedman et al 2006), suggesting vMCx sends commands to both start and stop a whisking epoch.…”

Section: Discussionmentioning

confidence: 90%

“…The activity of vMCx neurons does not co-vary with whisking frequency, suggesting that vMCx does not directly drive vMNs (Carvell et al 1996). Increased vMCx activity does, however, precede both the onset of whisking and changes in whisking kinematics (Friedman et al 2006). These observations are consistent with vMCx modulating the activity of a subcortical structure, such as serotonergic premotoneurons, to initiate and modulate whisking.…”

Section: Discussionmentioning

confidence: 96%

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The Whisking Rhythm Generator: A Novel Mammalian Network for the Generation of Movement

Cramer

Liu²,

Keller³

2007

Journal of Neurophysiology

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. Using the rat vibrissa system, we provide evidence for a novel mechanism for the generation of movement. Like other central pattern generators (CPGs) that underlie many movements, the rhythm generator for whisking can operate without cortical inputs or sensory feedback. However, unlike conventional mammalian CPGs, vibrissa motoneurons (vMNs) actively participate in the rhythmogenesis by converting tonic serotonergic inputs into the patterned motor output responsible for movement of the vibrissae. We find that, in vitro, a serotonin receptor agonist, ␣-Me-5HT, facilitates a persistent inward current (PIC) and evokes rhythmic firing in vMNs. Within each motoneuron, increasing the concentration of ␣-Me-5HT significantly increases the both the magnitude of the PIC and the motoneuron's firing rate. Riluzole, which selectively suppresses the Na ϩ component of PICs at low concentrations, causes a reduction in both of these phenomena. The magnitude of this reduction is directly correlated with the concentration of riluzole. The joint effects of riluzole on PIC magnitude and firing rate in vMNs suggest that the two are causally related. In vivo we find that the tonic activity of putative serotonergic premotoneurons is positively correlated with the frequency of whisking evoked by cortical stimulation. Taken together, these results support the hypothesized novel mammalian mechanism for movement generation in the vibrissa motor system where vMNs actively participate in the rhythmogenesis in response to tonic drive from serotonergic premotoneurons.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 96%

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The Whisking Rhythm Generator: A Novel Mammalian Network for the Generation of Movement

Cramer

Liu²,

Keller³

2007

Journal of Neurophysiology

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“…Prolonged preparatory neural activities characteristic to human voluntary actions are also found in diverse species including monkeys (Romo and Schultz, 1987;Kato et al, 1995;Kaufman et al, 2010) and rodents (Friedman et al, 2006); this suggests that the ability to self-initiate movement is a quantifiable biological trait shared across many vertebrate species including teleost fish. The experience of agency is essential for human volitional actions (Haggard, 2008), and the pre-supplementary motor area is shown to be activated when human subjects pay attention to their intention to act (Lau et al, 2004).…”

Section: Research Articlementioning

confidence: 99%

Enhanced sensory sampling precedes self-initiated locomotion in an electric fish

Jun

Longtin

Maler

2014

Journal of Experimental Biology

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Cortical activity precedes self-initiated movements by several seconds in mammals; this observation has led into inquiries on the nature of volition. Preparatory neural activity is known to be associated with decision making and movement planning. Selfinitiated locomotion has been linked to increased active sensory sampling; however, the precise temporal relationship between sensory acquisition and voluntary movement initiation has not been established. Based on long-term monitoring of sensory sampling activity that is readily observable in freely behaving pulse-type electric fish, we show that heightened sensory acquisition precedes spontaneous initiation of swimming. Gymnotus sp. revealed a bimodal distribution of electric organ discharge rate (EODR) demonstrating down-and up-states of sensory sampling and neural activity; movements only occurred during up-states and up-states were initiated before movement onset. EODR during voluntary swimming initiation exhibited greater trial-to-trial variability than the sound-evoked increases in EODR. The sampling variability declined after voluntary movement onset as previously observed for the neural variability associated with decision making in primates. Spontaneous movements occurred randomly without a characteristic timescale, and no significant temporal correlation was found between successive movement intervals. Using statistical analyses of spontaneous exploratory behaviours and associated preparatory sensory sampling increase, we conclude that electric fish exhibit key attributes of volitional movements, and that voluntary behaviours in vertebrates may generally be preceded by increased sensory sampling. Our results suggest that comparative studies of the neural basis of volition may therefore be possible in pulse-type electric fish, given the substantial homologies between the telencephali of teleost fish and mammals.

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“…As such, this procedure has enabled other difficult behavioral tasks (Gao et al, 2001;Bermejo et al, 2002;Gao et al, 2003b;Friedman et al, 2006) and intracellular (Crochet and Petersen, 2006) and extracellular (Sachdev et al, 2000;Kleinfeld et al, 2002;Melzer et al, 2006) recording studies. Yet it has been heretofore undocumented how head restraint may alter whisking behavior.…”

Section: Whisking In Head-fixed Versus Freely Exploring Animalsmentioning

confidence: 99%

Biomechanics of the Vibrissa Motor Plant in Rat: Rhythmic Whisking Consists of Triphasic Neuromuscular Activity

Hill¹,

Bermejo²,

Zeigler³

et al. 2008

J. Neurosci.

140

188

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The biomechanics of a motor plant constrain the behavioral strategies that an animal has available to extract information from its environment. We used the rat vibrissa system as a model for active sensing and determined the pattern of muscle activity that drives rhythmic exploratory whisking. Our approach made use of electromyography to measure the activation of all relevant muscles in both head-fixed and unrestrained rats and two-dimensional imaging to monitor the position of the vibrissae in head-fixed rats. Our essential finding is that the periodic motion of the vibrissae and mystacial pad during whisking results from three phases of muscle activity. First, the vibrissae are thrust forward as the rostral extrinsic muscle, musculus (m.) nasalis, contracts to pull the pad and initiate protraction. Second, late in protraction, the intrinsic muscles pivot the vibrissae farther forward. Third, retraction involves the cessation of m. nasalis and intrinsic muscle activity and the contraction of the caudal extrinsic muscles m. nasolabialis and m. maxillolabialis to pull the pad and the vibrissae backward. We developed a biomechanical model of the whisking motor plant that incorporates the measured muscular mechanics along with movement vectors observed from direct muscle stimulation in anesthetized rats. The results of simulations of the model quantify how the combination of extrinsic and intrinsic muscle activity leads to an enhanced range of vibrissa motion than would be available from the intrinsic muscles alone.

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Anticipatory Activity of Motor Cortex in Relation to Rhythmic Whisking

Cited by 27 publications

References 31 publications

The Whisking Rhythm Generator: A Novel Mammalian Network for the Generation of Movement

The Whisking Rhythm Generator: A Novel Mammalian Network for the Generation of Movement

Enhanced sensory sampling precedes self-initiated locomotion in an electric fish

Biomechanics of the Vibrissa Motor Plant in Rat: Rhythmic Whisking Consists of Triphasic Neuromuscular Activity

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