Exploratory Whisking by Rat Is Not Phase Locked to the Hippocampal Theta Rhythm

Berg, Rune W.; Whitmer, Diane; Kleinfeld, David

doi:10.1523/jneurosci.0190-06.2006

Cited by 35 publications

(30 citation statements)

References 32 publications

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“…Saccadic eye movements partition sensory input into discrete elements in much the same way that whisking and sniffing, behaviors often associated with hippocampal theta in rodents, break up somatosensory and olfactory information, respectively (1). Furthermore, the modulation of hippocampal activity by saccadic eye movements is reminiscent of previous findings showing that theta in rodents becomes phase-synchronized with whisking and sniffing during exploration (13,48) input (49), it suggests that one function of hippocampal theta across species may be as a mechanism to promote neural processing of information gathered during the performance of "sensing" behaviors.…”

Section: Discussionsupporting

confidence: 57%

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Jutras¹,

Fries

Buffalo

2013

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

244

266

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Primates explore the visual world through the use of saccadic eye movements. Neuronal activity in the hippocampus, a structure known to be essential for memory, is modulated by this saccadic activity, but the relationship between visual exploration through saccades and memory formation is not well understood. Here, we identify a link between theta-band (3-12 Hz) oscillatory activity in the hippocampus and saccadic activity in monkeys performing a recognition memory task. As monkeys freely explored novel images, saccades produced a theta-band phase reset, and the reliability of this phase reset was predictive of subsequent recognition. In addition, enhanced theta-band power before stimulus onset predicted stronger stimulus encoding. Together, these data suggest that hippocampal theta-band oscillations act in concert with active exploration in the primate and possibly serve to establish the optimal conditions for stimulus encoding.T he use of saccadic eye movements to acquire information about the surrounding environment is perhaps the most conspicuous example of exploratory behavior in the primate. This behavior provides a mechanism for parsing incoming information into discrete, stable segments (i.e., snapshots of individual elements comprising a complex visual scene, allowing time for sufficient processing to occur before moving to the next fixation target). This mechanism of actively sampling sensory information from the environment may be similar to the behaviors engaged in by rodents exploring their environment through such activities as sniffing and whisking. Specifically, the fixation period following each saccade may be homologous to the period of incoming sensory information accompanying each sniff cycle in the rodent (1). Recently, it has been suggested that motor behaviors associated with information gathering are integral to the "active sensing" process in natural behavior (2). It is plausible that there may exist certain common neuronal elements across species that are associated with active sensing processes, such that the neuronal mechanisms underlying the encoding of information are intimately connected with the motor activities involved in acquiring that information.In many mammalian species, voluntary, exploratory behaviors are often associated with theta-band activity, a prominent 3-to 12-Hz oscillatory activity in the hippocampus and other limbic structures. This activity has been studied extensively in the rodent hippocampus (3-5), but it has also been described in bats (6), cats (7), and, more recently, humans (8-11). In rodents, theta appears to show close temporal relationships with running (3, 12) and sniffing (13), suggesting an association between theta and the rate of sensory input. Although hippocampal theta has been identified in anesthetized monkeys (14), the lack of a clear demonstration of hippocampal theta in awake monkeys has been attributed to the fact that the recording methods typically require immobile, head-affixed monkeys, in contrast to rodent studies using freely moving ...

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Section: Discussionsupporting

confidence: 57%

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Jutras¹,

Fries

Buffalo

2013

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

244

266

View full text Add to dashboard Cite

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“…However, it has been shown in the rat whisker system that though the whisking frequency and hippocampal theta oscillations have the same frequencies, they are not synchronous 23 . We similarly determined the extent of correlation between the TC and LFP signals.…”

Section: Rats Track Various Odour Trails Accuratelymentioning

confidence: 96%

Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling

2012

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Tracking odour trails is a crucial behaviour for many animals, often leading to food, mates or away from danger. It is an excellent example of active sampling, where the animal itself controls how to sense the environment. Here we show that rats can track odour trails accurately with near-optimal sampling. We trained rats to follow odour trails drawn on paper spooled through a treadmill. By recording local field potentials (LFPs) from the olfactory bulb, and sniffing rates, we find that sniffing but not LFPs differ between tracking and non-tracking conditions. Rats can track odours within ~1 cm, and this accuracy is degraded when one nostril is closed. moreover, they show path prediction on encountering a fork, wide 'casting' sweeps on encountering a gap and detection of reappearance of the trail in 1-2 sniffs. We suggest that rats use a multi-layered strategy, and achieve efficient sampling and high accuracy in this complex task.

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“…Lesion studies have shown that whisking persists after sensory nerve transection (Welker, 1964;Gao et al, 2001;Berg and Kleinfeld, 2003;Berg et al, 2006), contralateral motor cortex ablation (Gao et al, 2003b), and extensive decerebration (Welker, 1964). These results argue for a brainstem central pattern generator to drive rhythmic whisking.…”

Section: Motor Control Of Exploratory Whiskingmentioning

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.

Self Cite

138

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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Exploratory Whisking by Rat Is Not Phase Locked to the Hippocampal Theta Rhythm

Cited by 35 publications

References 32 publications

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling

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

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